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Wheat fields as an ecological trap for reptiles in a semiarid agroecosystem
Biological Conservation 167 (2013) 349–353
Contents lists available at ScienceDirect
Biological Conservation journal homepage: www.elsevier.com/locate/biocon
Short communication
Wheat fields as an ecological trap for reptiles in a semiarid agroecosystem Guy Rotem a,c,⇑, Yaron Ziv a, Itamar Giladi a,b, Amos Bouskila c,b a
Spatial Ecology Lab, Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Israel c Behavioral Ecology Lab, Ben-Gurion University of the Negev, Beer-Sheva, Israel b
a r t i c l e
i n f o
Article history: Received 27 January 2013 Received in revised form 8 August 2013 Accepted 18 August 2013
Keywords: Agroecosystem Dispersal Ecological trap Fragmentation Habitat selection Trachylepis vittata
a b s t r a c t Intensive agricultural activity over large areas on earth, which is necessary to meet the increasing demand of a growing human population, may lead to biodiversity loss. This loss may be mitigated by keeping natural and semi-natural patches within agricultural fields to allow the maintenance of biological diversity (‘Wildlife Friendly Agriculture’). We conducted our study in an agroecosystem comprised of small isolated patches nested within agricultural fields. We trapped reptiles in 13 sampling sites, each of which included arrays of pitfall traps in a natural patch, in the adjacent wheat field and at the patch-field edge. We conducted six trapping sessions in the spring – four times before, once immediately after and once a week after the wheat harvest. Prior to the harvest, we found an intensive movement of Trachylepis vittata, the most common reptile in our study, from the semi-natural patches into the fields, but negligible movement in the opposite direction. This pre-harvest directional movement corresponded with higher abundance of prey (i.e., arthropods) in the wheat field compared to the natural patches in early spring. The individuals that moved into the fields were adults of better body condition than those remaining in the patch, suggesting that the motivation for movement was habitat preference by individuals with high prospective fitness rather than the exclusion of subordinates. The population of T. vittata in the wheat fields and movement across habitats dropped to zero during and after the harvest. Our results provide strong evidence that the agricultural fields serve as an ecological trap to organisms inhabiting nearby natural habitats. We suggest that plans for Wildlife-Friendly Agriculture for biodiversity conservation should consider also potential negative effects, such as the ecological trap effect. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction A rapidly growing global human population coupled with an increase in per-capita consumption challenge modern agriculture to increase productivity in order to meet the increasing demand. This challenge is being tackled by both an expansion of farming area and an intensification of agricultural practices. The vast terrestrial areas affected by agriculture (about 80% globally; MEA, 2005), agricultural intensification, and the cultivation of monocultures are all expected to cause biodiversity loss (FAO, 2007; Green et al., 2005). One recent approach to alleviate the negative effects of agriculture on biodiversity is ‘Wildlife Friendly Agriculture’, which apparently promotes a balance between food production and conservation by, among others, leaving natural habitat patches within a heteroge⇑ Corresponding author. Address: Department of Life Sciences, Ben-Gurion University of the Negev, P.O.B. 653, Beer-Sheva 84105, Israel. Tel.: +972 8 6461350, mobile: +972 52 3354485; fax: +972 8 6479221. E-mail addresses: [email protected] (G. Rotem), [email protected] (Y. Ziv), [email protected] (I. Giladi), [email protected] (A. Bouskila). 0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.08.028
neous agricultural landscape (Green et al., 2005). Accordingly, preservation of natural or semi-natural patches within the agricultural matrix is considered an effective and relatively cheap way to preserve biodiversity (Aarssen and Schamp, 2002; Benton et al., 2003; Duelli and Obrist, 2003). In addition to biodiversity conservation, this approach may be beneficial also for farmers because of the positive ecosystem services that natural habitats provide for agriculture (Rosenzweig, 2003a,b; Tscharntke et al., 2005; Bommarco et al., 2013). However, the proximity of natural habitat patches to agricultural matrix may also affect animal behavior, in general, and habitat selection, in particular (Tscharntke et al., 2012). The selection of habitats in which to shelter, feed and reproduce can dramatically impact organism fitness. Consequently, most animals have evolved abilities to sense reliable cues regarding habitat quality and to move to a better habitat whenever possible (Abramsky et al., 1985; Pulliam, 1988). However, the ability to reliably assess habitat quality is often compromised in human-made environments (Kristan, 2003; Battin, 2004). Cultivation-related fluctuation in habitat quality
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may attract individuals at certain times and be detrimental at other times (Best, 1986; Bollinger et al., 1990). The case where an organism prefers low-quality habitats over other available better habitats is called an ‘ecological trap’ (Dwernych and Boag, 1972; Donovan and Thompson, 2001; Hawlena et al., 2010), which might be considered a special case of source-sink dynamics (Pulliam, 1988; Battin, 2004). Such ecological traps may have farreaching consequences for the populations in both the low and the high quality habitats. Robertson and Hutto, (2006) offer three criteria that define an ‘ecological trap’: ‘‘(1) individuals should have exhibited a preference for one habitat over another; (2) a reasonable surrogate measure of individual fitness should have differed among habitats; and (3) the fitness outcome for individuals settling in the preferred habitat must have been lower than the fitness attained in other available habitat’’. Our study area, the Beit-Nir agroecosystem, is located at the northern part of Southern Judea Lowlands (SJL), central Israel (31°300 5200 N 34°520 3600 E), approximately 50 km southwest of Jerusalem (Fig. 1a). Thousands of years of human inhabitance (Ben-Yosef, 1980) and recent intensive agricultural practice formed a landscape consisting of natural habitat patches at different degrees of isolation, surrounded by agricultural fields (mainly wheat) vineyards and olive groves. The presence of semi-natural patches within this agricultural landscape can potentially host a high diversity of reptiles. However, these patches are positioned within wheat fields, a habitat with potentially highly fluctuating quality due to seasonal cultivation. Using reptiles, we examine the main hypothesis that the agricultural system serves as an ecological trap, as defined by Robertson and Hutto (2006), where many individuals move to and permanently occupy the agricultural fields, eliminated by the agricultural machinery before or during the reproduction season. We contrast this hypothesis with an alternative one, stating that the agricultural system is used for a daily foraging ground by individuals that mainly occupy the adjacent natural habitats. Our model species Trachylepis vittata [Scincidae] is common along the eastern Mediterranean basin and in North Africa (Van der Winden et al., 1995). It is frequently found under stones in the early morning until the ambient temperature rises above 14 °C. This species also uses rocks as shelters to escape rain and other extreme weather (Clark and Clark, 1973). It measures 225 mm from snout to tail and feeds on arthropods (Schleich et al., 1996). Females give birth to live offspring between July and August (Disi et al., 2001, p. 226).
2. Methods 2.1. Study design and survey protocol We surveyed reptiles in 13 sampling sites, each including a natural patch, an adjacent wheat field and the patch-field edge (Fig. 1b). At each site we installed 40 traps, positioned in two arrays, each comprised of 20 one-liter dry pitfall traps. The traps were arranged in two parallel lines at distances of 10 m and 15 m on either side of the patch-field edge (Fig. 1b). Additionally, on the patch-field edge we used a polypropylene multiwall sheet to build a 100 m-long and 40 cm-high fence (Fig. 1b) that directs all reptiles’ movement between the natural patch and the agricultural field to passageways located every 20 m along the fence (Fisher et al., 2008). At those passageways we placed two one-liter dry pitfall traps, one at each side (total of 10 one-liter dry pitfall traps along each fence). These sampling methods enabled us to simultaneously asses the community structure and monitor the physical condition of reptiles in the natural patch, in the field,
while crossing from the natural patch to field and while crossing in the opposite direction (Jenkins and McGarigal, 2003). We trapped reptiles during six sessions throughout the spring (March to June) – four times before the wheat harvest, immediately after the harvest and one week later. In each session, traps were left open for 72 h. Trapped animals were measured (i.e. weight, snout-to-vent-length, tail length) and identified to species (and sex when possible; see results). Individuals’ physical condition was assessed by an index of body condition (IC; Andrews and Wright, 1994). Initially we intended on using individual marking to follow the reptiles’ movement. However, as marking of individuals during the four first sampling sessions resulted in no recapture at all, this method was not used further on. We released all captured individuals back to the habitat where they were captured (in the natural patch or agricultural field) or to the habitat they were aiming for (in the patch-field edge). We averaged all the observations from each combination of ‘habitat’ ‘session’ ‘site’ prior to any statistical analysis and used these summarized data as our replicates, thus avoiding any pseudo-replication. Incidentally, the pitfall traps also collected arthropods that were later identified in the lab to their order level. Previous studies have found a positive correlation between insect abundance and reptile abundance (Rocha et al., 2008). As all the studied reptile species were predators, having insects as a dominant component of their diet, we assumed that arthropod abundance could serve as a good indicator for habitat quality.
3. Results Throughout the study, we trapped 352 reptiles, belonging to 9 species. Most of the trapped individuals (271) belonged to our model species, T. vittata. The vast majority (244) of the 271 individuals of T. vittata, throughout the season and in all habitat types were adults, 16 were sub-adults (mainly in the pre-harvest sessions only, and in all habitat types) and only 11 were juveniles, all of which were captured in the natural patch habitat in the post-harvest session. Although it was sometimes possible to determine the sex of trapped individuals, in most cases it could not be reliably done. Therefore, our analysis was not stratified by sex or by age. We found a significant effect of both sampling time and habitat (repeated-measures ANOVA, F(5, 240) = 10.43, p < 0.001, and F(3, 48) = 72.46, p < 0.001, respectively) as well as their interaction (F(15, 240) = 9.0643, p < 0.0001) on T. vittata’s abundance (Fig. 2). T. vittata abundance (Fig. 2) in natural patches remained relatively constant throughout the entire study period. In contrast, the number of T. vittata found in the wheat field varied. Early in the season only a few individuals occurred within the field habitat, but their number increased throughout the spring until the harvest. After the wheat harvest, not a single individual was found within the field habitat. The reptiles’ movement across habitats was unidirectional with an intensive movement from the natural patches into the wheat fields in early spring (38 individuals observed). Only two individuals attempted crossing in the opposite direction throughout the entire season. The very low densities of other reptile species precluded us from conducting meaningful analyses at the species level. Nevertheless, the general patterns for all the rest of the reptile community combined was similar to the results found for T. vittata. The number of reptiles (excluding T. vittata) captured per trapping array per session remained constant in the natural patch habitat throughout the season (0.69 and 0.77 for pre-harvest and post-harvest, respectively). It dropped sharply in the field habitat (from 0.25 individuals in the pre-harvest to 0 in the post-harvest). Prior to the harvest, twice as many individuals crossed from the patch to the field than in the opposite
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Fig. 1. Map of the research area and the study site. (a) White polygons represent natural and semi-natural patches surrounded by agricultural fields, mainly wheat. A diagram of a trapping array and (b) showing the fence (black line) and the trapping array in each habitat and along the separating fence. A picture of the patch-field edge and the separating fence is given in c.
the natural habitat to the agricultural field (p = 0.0001, Tukey’s honestly significant difference post hoc test). All individuals in the field and those crossing from the natural patch to the field were adults, whereas juveniles and newborn were found in the natural patches only. In early spring arthropod abundance within the wheat fields was significantly higher compared to that in the natural patches (in early spring: t-test, t17 = 3.791, p = 0.001, SD = 77.173; after the harvest arthropod abundance within the wheat fields was not significantly different than that in the natural patches: t-test, t17 = 1.912, p = 0.07, SD = 72.115). 4. Discussion
Fig. 2. Mean number of Trachylepis vittata individuals per trapping array that was captured in natural patches, wheat fields and while crossing between these habitats at different times along the wheat growing season. T. vittata was captured in four occasions prior to the wheat harvest (Pre-H1–H4 corresponding to end of February, end of March, Mid April and end of May), immediately after the harvest (Harvest) and one week later (post-H).
direction (0.15 and 0.08 individuals per trapping array per session, respectively) and no movement was observed in either direction after the harvest. Habitat type significantly affected body condition of T. vittata (Fig. 3; one-way ANOVA, F(2, 61) = 33.7, p < 0.05) and we found that individuals in the natural patches were in poorer physical condition than those captured in the field or those striving to cross from
Robertson and Hutto (2006) criteria for the existence of an ecological trap include preference for one habitat over another and lower fitness (measured directly or using a surrogate) in the preferred relative to the other habitat (see Introduction). The relatively higher insect abundance in the field in early spring may explain the extreme asymmetrical movement of individuals of the insectivorous skink, T. vittata, from the natural patches to the field. Furthermore, the superior body condition of adults crossing to, or already in the field, relative to those remaining in the natural patches, clearly indicates that the movement to the habitat with high food abundance is mainly executed by the individuals in a better condition, with high potential for reproduction. Meylan et al. (2002) showed that when movement between patches (i.e., dispersal) incurs a high energetic cost, only individuals of better body condition make an attempt for such movement. Whether or not this mechanism drove our results, the superior body condi-
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Fig. 3. Index of body condition (IC index) of individuals in the fields, natural patches and along the fence separating patch and field. The analysis is based on early-spring trapped adults with intact tail.
tioned individuals clearly showed preference to the agricultural field. Combined our observations suggest that in early spring, individuals behave according to the expectation of ideal density-dependent habitat selection (Fretwell and Lucas, 1969), i.e., moving to a higher quality habitat to increase fitness. However, this seemingly optimal habitat selection eventually led individuals to be trapped in a very poor habitat following the wheat harvest. We have not found even a single live T. vittata in the field following the harvest activity. Furthermore, we have not found evidence of movement of any individual from the field into the patch during or after the harvest, nor immediately prior to the harvest, despite a buildup of substantial population in the field at this time (Fig. 2). Some of the reptiles in the field were presumably killed by the agricultural machinery; others, exposed to predators like Corvus monedula, Falco tinnunculus or Circaetus gallicus that accompanied the harvest activity, were likely consumed. We indeed counted more than 20 individuals of each of these predatory birds following the harvester, apparently collecting prey uncovered by the harvester (personal observations). This phenomenal scene is typical to harvesting activity throughout SJL and Israel, and, as far as we know, also throughout the world. Much of the results that we obtained, at least early in the season, could have been generated by a daily movement of individuals that reside and reproduce in the natural patch and conduct daily foraging forays into the fields where they benefit from the high arthropod abundance. If that was the case, we would expect that at least some individuals that arrived during a trapping session will be captured on their return to the natural patch. The almost complete lack of such movement, especially in the last session prior to the harvest, when substantial population was found in the field, clearly rejects the daily pattern hypothesis. Furthermore, throughout the spring, the T. vittata population within the agricultural field grew, which could indicate that individuals that moved from the natural patches remained in the field and have not used it just for diurnal foraging. Finally, if daily foraging individuals benefited from high quality food in the fields, one could expect a negative correlation between the physical state of individuals in natural patches and the distance from the high quality field habitat. Using auxiliary data, where traps were located in different distances from the patch-field edge (Rotem, 2012), we found no such correlation (Linear regression, F1,34 = 1.10, p = 0.30, R2 = 0.03). Clearly, our results and observations indicate a large difference between the fitness provided by the two habitats – while reproduction of T. vittata occurs in the natural patch (as evident by the
observation of a few newborns late in the season after the harvest), the fitness in the fields equals zero (not even a single live T. vittata, adult or juvenile, in the field following the harvest activity). Following the criteria set by Robertson and Hutto, (2006), we affirm that the agricultural fields serve as an ecological trap for T. vittata – better-conditioned individuals show preference for the field, as indicated by their directionality of movement; the field offers higher resource quantity indicating a potential difference in prospective fitness; and the preferred habitat has eventually a lower fitness. Although the data enabled us to conduct detailed analysis for only one common species, the similar patterns observed for the rest of the community suggest that the implications of the results may be pertinent for many species, including rare species for which data is always hard to obtain. Organisms make decisions regarding their future success based on currently available information. Most of these decisions are based on the long process of evolutionary promotion of optimal habitat selection (Schlaepfer et al., 2002). However, adaptations for optimal habitat selection that have been shaped by long-term evolutionary processes may be out of context in cases of anthropogenic intervention with the natural environment (Hawlena et al., 2010). Such intervention, which is usually much faster than almost any evolutionary process, leads to situations in which organisms select habitats according to their ‘‘evolutionary knowledge’’ (Battin, 2004), leading, on occasions, to ecological traps (e.g., Hawlena et al., 2010). In our case, the wheat field serves as an ecological trap by attracting individuals of better physical condition in the population to migrate to the seemingly better habitat. These individuals, of high prospective fitness, find themselves in a very poor habitat after the harvest, leading to no fitness at all. The passage of individuals in better physical condition from the natural patches into the wheat fields, where their fitness is very low, may further decrease both population size and the quality of the natural patches’ populations (Schlaepfer et al., 2002). Small fragmented populations are exposed to inbreeding depression and genetic drift, which further decrease the population’s genetic diversity and weaken its ability to cope with both short-term stochasticity (e.g., drought period) and long-term environmental change (Porlier et al., 2009). The effects of genetic isolation and the negative qualitative and quantitative effects of ecological traps on isolated populations in natural patches may be additive, or even synergistic, increasing the probability of extinction for those populations. The asymmetric, almost unidirectional, movement across habitats and the functioning of the wheat fields as an ecological trap pose a risk, particularly to small patches that share a long border with the fields relative to their patch area. In such small patches, the loss of individuals that do not reproduce in the patch may be detrimental, due to the reduction in the number of individuals available to replace natural mortality in the patch and due to potentially gradual loss in the quality of the remaining individuals in the patch. We believe that the phenomenon of an ecological trap in agroecosystems is not unique to our study area or to our study species, but may represent an example of a broad phenomenon, probably found in agricultural areas in many places worldwide (see Bollinger et al., 1990; Shochat et al., 2005). Consequently, we think that possible risks of ecological traps should be incorporated in the ‘Wildlife Friendly Agriculture’ approach (see Introduction) that is currently proposed to promote conservation.
Acknowledgements This study was funded by Nekudat Hen foundation. This research was also partially supported by a grant from the Israel Science Foundation (ISF grant 751/09) to Y.Z. We thank our assistants,
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especially Gal Aviad, for their help in the field and the farmers of Kibutz Bet-Nir for their cooperation. This study was conducted under Israel National Parks Authority permit number 2011/38096. References Aarssen, L.W., Schamp, B.S., 2002. Predicting distributions of species richness and species size in regional floras: applying the species pool hypothesis to the habitat templet model. Perspect. Plant Ecol. Evol. Syst. 5, 3–12. Abramsky, Z., Rosenzweig, M.L., Brand, S., 1985. Habitat selection of Israel desert rodents – comparison of a traditional and a new method of analysis. Oikos 45, 79–88. Andrews, R.M., Wright, S.J., 1994. Long-term population fluctuations of a tropical lizard: a test of causality. In: Vitt, L.L., Pianka, E.R. (Eds.), Lizard Ecology Historical and Experimental Perspective. Princeton University Press, New Jersey, pp. 267–285. Battin, J., 2004. When good animals love bad habitats: ecological traps and the conservation of animal populations. Conservat. Biol. 18, 1482–1491. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188. Ben-Yosef, S., 1980. Israel Guide (vol. Judea). Keter Publishing House, Jerusalem (In Hebrew). Best, L.B., 1986. Conservation Tillage: Ecological Traps for Nesting Birds? Wildlife Soc. Bull. 14, 308–317. Bollinger, E.K., Bollinger, P.B., Gavin, T.A., 1990. Effects of hay-cropping on eastern populations of the bobolink. Wildlife Soc. Bull. 18, 142–150. Bommarco, R., Kleijn, D., Potts, S.G., 2013. Ecological intensification: harnessing ecosystem services for food security. Trends in Ecol. Evol. 28, 230–238. Clark, R.J., Clark, E.D., 1973. Report on a collection of amphibians and reptiles from Thrkey, In Occasional papers of the California Academy of Sciences. Disi, M. Ahmad., Mordry, D., Necas, P., Rifai, L, 2001. Amphibians and Reptiles of the Hashemite Kingdom of Jordan, An Atlas and Field Guide. Edition Chimaira. Donovan, T.M., Thompson, F.R., 2001. Modeling the ecological trap hypothesis: a habitat and demographic analysis for migrant songbirds. Ecol. Appl. 11, 871– 882. Duelli, P., Obrist, M.K., 2003. Regional biodiversity in an agricultural landscape: the contribution of semi-natural habitat islands. Basic Appl. Ecol. 4, 129–138. Dwernych, L.W., Boag, D.A., 1972. Ducks nesting in association with gulls – ecological trap. Can. J. Zool. 50, 559–563. FAO (Food and Agriculture Organization of the United Nations). 2007. The state of food and agriculture paying farmers for environmental services. Food and Agriculture Organization of the United Nations, FAO Agriculture Series No. 38. Fisher, R., Stokes, D., Rochester, C., Brehme, C., Hathaway, S., Case, T., 2008. Herpetological monitoring using a pitfall trapping design in southern California. U.S. Geological Survey Techniques and Methods 2–A5. Fretwell, S.D., Lucas, H.L., 1969. On territorial behavior and other factors influencing habitat distribution in birds. Theor. Develop. Acta Biotheor. 19, 16–36. Green, R.E., Cornell, S.J., Scharlemann, J.P.W., Balmford, A., 2005. Farming and the fate of wild nature. Science 307, 550–555.
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Contents lists available at ScienceDirect
Biological Conservation journal homepage: www.elsevier.com/locate/biocon
Short communication
Wheat fields as an ecological trap for reptiles in a semiarid agroecosystem Guy Rotem a,c,⇑, Yaron Ziv a, Itamar Giladi a,b, Amos Bouskila c,b a
Spatial Ecology Lab, Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Israel c Behavioral Ecology Lab, Ben-Gurion University of the Negev, Beer-Sheva, Israel b
a r t i c l e
i n f o
Article history: Received 27 January 2013 Received in revised form 8 August 2013 Accepted 18 August 2013
Keywords: Agroecosystem Dispersal Ecological trap Fragmentation Habitat selection Trachylepis vittata
a b s t r a c t Intensive agricultural activity over large areas on earth, which is necessary to meet the increasing demand of a growing human population, may lead to biodiversity loss. This loss may be mitigated by keeping natural and semi-natural patches within agricultural fields to allow the maintenance of biological diversity (‘Wildlife Friendly Agriculture’). We conducted our study in an agroecosystem comprised of small isolated patches nested within agricultural fields. We trapped reptiles in 13 sampling sites, each of which included arrays of pitfall traps in a natural patch, in the adjacent wheat field and at the patch-field edge. We conducted six trapping sessions in the spring – four times before, once immediately after and once a week after the wheat harvest. Prior to the harvest, we found an intensive movement of Trachylepis vittata, the most common reptile in our study, from the semi-natural patches into the fields, but negligible movement in the opposite direction. This pre-harvest directional movement corresponded with higher abundance of prey (i.e., arthropods) in the wheat field compared to the natural patches in early spring. The individuals that moved into the fields were adults of better body condition than those remaining in the patch, suggesting that the motivation for movement was habitat preference by individuals with high prospective fitness rather than the exclusion of subordinates. The population of T. vittata in the wheat fields and movement across habitats dropped to zero during and after the harvest. Our results provide strong evidence that the agricultural fields serve as an ecological trap to organisms inhabiting nearby natural habitats. We suggest that plans for Wildlife-Friendly Agriculture for biodiversity conservation should consider also potential negative effects, such as the ecological trap effect. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction A rapidly growing global human population coupled with an increase in per-capita consumption challenge modern agriculture to increase productivity in order to meet the increasing demand. This challenge is being tackled by both an expansion of farming area and an intensification of agricultural practices. The vast terrestrial areas affected by agriculture (about 80% globally; MEA, 2005), agricultural intensification, and the cultivation of monocultures are all expected to cause biodiversity loss (FAO, 2007; Green et al., 2005). One recent approach to alleviate the negative effects of agriculture on biodiversity is ‘Wildlife Friendly Agriculture’, which apparently promotes a balance between food production and conservation by, among others, leaving natural habitat patches within a heteroge⇑ Corresponding author. Address: Department of Life Sciences, Ben-Gurion University of the Negev, P.O.B. 653, Beer-Sheva 84105, Israel. Tel.: +972 8 6461350, mobile: +972 52 3354485; fax: +972 8 6479221. E-mail addresses: [email protected] (G. Rotem), [email protected] (Y. Ziv), [email protected] (I. Giladi), [email protected] (A. Bouskila). 0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.08.028
neous agricultural landscape (Green et al., 2005). Accordingly, preservation of natural or semi-natural patches within the agricultural matrix is considered an effective and relatively cheap way to preserve biodiversity (Aarssen and Schamp, 2002; Benton et al., 2003; Duelli and Obrist, 2003). In addition to biodiversity conservation, this approach may be beneficial also for farmers because of the positive ecosystem services that natural habitats provide for agriculture (Rosenzweig, 2003a,b; Tscharntke et al., 2005; Bommarco et al., 2013). However, the proximity of natural habitat patches to agricultural matrix may also affect animal behavior, in general, and habitat selection, in particular (Tscharntke et al., 2012). The selection of habitats in which to shelter, feed and reproduce can dramatically impact organism fitness. Consequently, most animals have evolved abilities to sense reliable cues regarding habitat quality and to move to a better habitat whenever possible (Abramsky et al., 1985; Pulliam, 1988). However, the ability to reliably assess habitat quality is often compromised in human-made environments (Kristan, 2003; Battin, 2004). Cultivation-related fluctuation in habitat quality
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may attract individuals at certain times and be detrimental at other times (Best, 1986; Bollinger et al., 1990). The case where an organism prefers low-quality habitats over other available better habitats is called an ‘ecological trap’ (Dwernych and Boag, 1972; Donovan and Thompson, 2001; Hawlena et al., 2010), which might be considered a special case of source-sink dynamics (Pulliam, 1988; Battin, 2004). Such ecological traps may have farreaching consequences for the populations in both the low and the high quality habitats. Robertson and Hutto, (2006) offer three criteria that define an ‘ecological trap’: ‘‘(1) individuals should have exhibited a preference for one habitat over another; (2) a reasonable surrogate measure of individual fitness should have differed among habitats; and (3) the fitness outcome for individuals settling in the preferred habitat must have been lower than the fitness attained in other available habitat’’. Our study area, the Beit-Nir agroecosystem, is located at the northern part of Southern Judea Lowlands (SJL), central Israel (31°300 5200 N 34°520 3600 E), approximately 50 km southwest of Jerusalem (Fig. 1a). Thousands of years of human inhabitance (Ben-Yosef, 1980) and recent intensive agricultural practice formed a landscape consisting of natural habitat patches at different degrees of isolation, surrounded by agricultural fields (mainly wheat) vineyards and olive groves. The presence of semi-natural patches within this agricultural landscape can potentially host a high diversity of reptiles. However, these patches are positioned within wheat fields, a habitat with potentially highly fluctuating quality due to seasonal cultivation. Using reptiles, we examine the main hypothesis that the agricultural system serves as an ecological trap, as defined by Robertson and Hutto (2006), where many individuals move to and permanently occupy the agricultural fields, eliminated by the agricultural machinery before or during the reproduction season. We contrast this hypothesis with an alternative one, stating that the agricultural system is used for a daily foraging ground by individuals that mainly occupy the adjacent natural habitats. Our model species Trachylepis vittata [Scincidae] is common along the eastern Mediterranean basin and in North Africa (Van der Winden et al., 1995). It is frequently found under stones in the early morning until the ambient temperature rises above 14 °C. This species also uses rocks as shelters to escape rain and other extreme weather (Clark and Clark, 1973). It measures 225 mm from snout to tail and feeds on arthropods (Schleich et al., 1996). Females give birth to live offspring between July and August (Disi et al., 2001, p. 226).
2. Methods 2.1. Study design and survey protocol We surveyed reptiles in 13 sampling sites, each including a natural patch, an adjacent wheat field and the patch-field edge (Fig. 1b). At each site we installed 40 traps, positioned in two arrays, each comprised of 20 one-liter dry pitfall traps. The traps were arranged in two parallel lines at distances of 10 m and 15 m on either side of the patch-field edge (Fig. 1b). Additionally, on the patch-field edge we used a polypropylene multiwall sheet to build a 100 m-long and 40 cm-high fence (Fig. 1b) that directs all reptiles’ movement between the natural patch and the agricultural field to passageways located every 20 m along the fence (Fisher et al., 2008). At those passageways we placed two one-liter dry pitfall traps, one at each side (total of 10 one-liter dry pitfall traps along each fence). These sampling methods enabled us to simultaneously asses the community structure and monitor the physical condition of reptiles in the natural patch, in the field,
while crossing from the natural patch to field and while crossing in the opposite direction (Jenkins and McGarigal, 2003). We trapped reptiles during six sessions throughout the spring (March to June) – four times before the wheat harvest, immediately after the harvest and one week later. In each session, traps were left open for 72 h. Trapped animals were measured (i.e. weight, snout-to-vent-length, tail length) and identified to species (and sex when possible; see results). Individuals’ physical condition was assessed by an index of body condition (IC; Andrews and Wright, 1994). Initially we intended on using individual marking to follow the reptiles’ movement. However, as marking of individuals during the four first sampling sessions resulted in no recapture at all, this method was not used further on. We released all captured individuals back to the habitat where they were captured (in the natural patch or agricultural field) or to the habitat they were aiming for (in the patch-field edge). We averaged all the observations from each combination of ‘habitat’ ‘session’ ‘site’ prior to any statistical analysis and used these summarized data as our replicates, thus avoiding any pseudo-replication. Incidentally, the pitfall traps also collected arthropods that were later identified in the lab to their order level. Previous studies have found a positive correlation between insect abundance and reptile abundance (Rocha et al., 2008). As all the studied reptile species were predators, having insects as a dominant component of their diet, we assumed that arthropod abundance could serve as a good indicator for habitat quality.
3. Results Throughout the study, we trapped 352 reptiles, belonging to 9 species. Most of the trapped individuals (271) belonged to our model species, T. vittata. The vast majority (244) of the 271 individuals of T. vittata, throughout the season and in all habitat types were adults, 16 were sub-adults (mainly in the pre-harvest sessions only, and in all habitat types) and only 11 were juveniles, all of which were captured in the natural patch habitat in the post-harvest session. Although it was sometimes possible to determine the sex of trapped individuals, in most cases it could not be reliably done. Therefore, our analysis was not stratified by sex or by age. We found a significant effect of both sampling time and habitat (repeated-measures ANOVA, F(5, 240) = 10.43, p < 0.001, and F(3, 48) = 72.46, p < 0.001, respectively) as well as their interaction (F(15, 240) = 9.0643, p < 0.0001) on T. vittata’s abundance (Fig. 2). T. vittata abundance (Fig. 2) in natural patches remained relatively constant throughout the entire study period. In contrast, the number of T. vittata found in the wheat field varied. Early in the season only a few individuals occurred within the field habitat, but their number increased throughout the spring until the harvest. After the wheat harvest, not a single individual was found within the field habitat. The reptiles’ movement across habitats was unidirectional with an intensive movement from the natural patches into the wheat fields in early spring (38 individuals observed). Only two individuals attempted crossing in the opposite direction throughout the entire season. The very low densities of other reptile species precluded us from conducting meaningful analyses at the species level. Nevertheless, the general patterns for all the rest of the reptile community combined was similar to the results found for T. vittata. The number of reptiles (excluding T. vittata) captured per trapping array per session remained constant in the natural patch habitat throughout the season (0.69 and 0.77 for pre-harvest and post-harvest, respectively). It dropped sharply in the field habitat (from 0.25 individuals in the pre-harvest to 0 in the post-harvest). Prior to the harvest, twice as many individuals crossed from the patch to the field than in the opposite
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Fig. 1. Map of the research area and the study site. (a) White polygons represent natural and semi-natural patches surrounded by agricultural fields, mainly wheat. A diagram of a trapping array and (b) showing the fence (black line) and the trapping array in each habitat and along the separating fence. A picture of the patch-field edge and the separating fence is given in c.
the natural habitat to the agricultural field (p = 0.0001, Tukey’s honestly significant difference post hoc test). All individuals in the field and those crossing from the natural patch to the field were adults, whereas juveniles and newborn were found in the natural patches only. In early spring arthropod abundance within the wheat fields was significantly higher compared to that in the natural patches (in early spring: t-test, t17 = 3.791, p = 0.001, SD = 77.173; after the harvest arthropod abundance within the wheat fields was not significantly different than that in the natural patches: t-test, t17 = 1.912, p = 0.07, SD = 72.115). 4. Discussion
Fig. 2. Mean number of Trachylepis vittata individuals per trapping array that was captured in natural patches, wheat fields and while crossing between these habitats at different times along the wheat growing season. T. vittata was captured in four occasions prior to the wheat harvest (Pre-H1–H4 corresponding to end of February, end of March, Mid April and end of May), immediately after the harvest (Harvest) and one week later (post-H).
direction (0.15 and 0.08 individuals per trapping array per session, respectively) and no movement was observed in either direction after the harvest. Habitat type significantly affected body condition of T. vittata (Fig. 3; one-way ANOVA, F(2, 61) = 33.7, p < 0.05) and we found that individuals in the natural patches were in poorer physical condition than those captured in the field or those striving to cross from
Robertson and Hutto (2006) criteria for the existence of an ecological trap include preference for one habitat over another and lower fitness (measured directly or using a surrogate) in the preferred relative to the other habitat (see Introduction). The relatively higher insect abundance in the field in early spring may explain the extreme asymmetrical movement of individuals of the insectivorous skink, T. vittata, from the natural patches to the field. Furthermore, the superior body condition of adults crossing to, or already in the field, relative to those remaining in the natural patches, clearly indicates that the movement to the habitat with high food abundance is mainly executed by the individuals in a better condition, with high potential for reproduction. Meylan et al. (2002) showed that when movement between patches (i.e., dispersal) incurs a high energetic cost, only individuals of better body condition make an attempt for such movement. Whether or not this mechanism drove our results, the superior body condi-
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Fig. 3. Index of body condition (IC index) of individuals in the fields, natural patches and along the fence separating patch and field. The analysis is based on early-spring trapped adults with intact tail.
tioned individuals clearly showed preference to the agricultural field. Combined our observations suggest that in early spring, individuals behave according to the expectation of ideal density-dependent habitat selection (Fretwell and Lucas, 1969), i.e., moving to a higher quality habitat to increase fitness. However, this seemingly optimal habitat selection eventually led individuals to be trapped in a very poor habitat following the wheat harvest. We have not found even a single live T. vittata in the field following the harvest activity. Furthermore, we have not found evidence of movement of any individual from the field into the patch during or after the harvest, nor immediately prior to the harvest, despite a buildup of substantial population in the field at this time (Fig. 2). Some of the reptiles in the field were presumably killed by the agricultural machinery; others, exposed to predators like Corvus monedula, Falco tinnunculus or Circaetus gallicus that accompanied the harvest activity, were likely consumed. We indeed counted more than 20 individuals of each of these predatory birds following the harvester, apparently collecting prey uncovered by the harvester (personal observations). This phenomenal scene is typical to harvesting activity throughout SJL and Israel, and, as far as we know, also throughout the world. Much of the results that we obtained, at least early in the season, could have been generated by a daily movement of individuals that reside and reproduce in the natural patch and conduct daily foraging forays into the fields where they benefit from the high arthropod abundance. If that was the case, we would expect that at least some individuals that arrived during a trapping session will be captured on their return to the natural patch. The almost complete lack of such movement, especially in the last session prior to the harvest, when substantial population was found in the field, clearly rejects the daily pattern hypothesis. Furthermore, throughout the spring, the T. vittata population within the agricultural field grew, which could indicate that individuals that moved from the natural patches remained in the field and have not used it just for diurnal foraging. Finally, if daily foraging individuals benefited from high quality food in the fields, one could expect a negative correlation between the physical state of individuals in natural patches and the distance from the high quality field habitat. Using auxiliary data, where traps were located in different distances from the patch-field edge (Rotem, 2012), we found no such correlation (Linear regression, F1,34 = 1.10, p = 0.30, R2 = 0.03). Clearly, our results and observations indicate a large difference between the fitness provided by the two habitats – while reproduction of T. vittata occurs in the natural patch (as evident by the
observation of a few newborns late in the season after the harvest), the fitness in the fields equals zero (not even a single live T. vittata, adult or juvenile, in the field following the harvest activity). Following the criteria set by Robertson and Hutto, (2006), we affirm that the agricultural fields serve as an ecological trap for T. vittata – better-conditioned individuals show preference for the field, as indicated by their directionality of movement; the field offers higher resource quantity indicating a potential difference in prospective fitness; and the preferred habitat has eventually a lower fitness. Although the data enabled us to conduct detailed analysis for only one common species, the similar patterns observed for the rest of the community suggest that the implications of the results may be pertinent for many species, including rare species for which data is always hard to obtain. Organisms make decisions regarding their future success based on currently available information. Most of these decisions are based on the long process of evolutionary promotion of optimal habitat selection (Schlaepfer et al., 2002). However, adaptations for optimal habitat selection that have been shaped by long-term evolutionary processes may be out of context in cases of anthropogenic intervention with the natural environment (Hawlena et al., 2010). Such intervention, which is usually much faster than almost any evolutionary process, leads to situations in which organisms select habitats according to their ‘‘evolutionary knowledge’’ (Battin, 2004), leading, on occasions, to ecological traps (e.g., Hawlena et al., 2010). In our case, the wheat field serves as an ecological trap by attracting individuals of better physical condition in the population to migrate to the seemingly better habitat. These individuals, of high prospective fitness, find themselves in a very poor habitat after the harvest, leading to no fitness at all. The passage of individuals in better physical condition from the natural patches into the wheat fields, where their fitness is very low, may further decrease both population size and the quality of the natural patches’ populations (Schlaepfer et al., 2002). Small fragmented populations are exposed to inbreeding depression and genetic drift, which further decrease the population’s genetic diversity and weaken its ability to cope with both short-term stochasticity (e.g., drought period) and long-term environmental change (Porlier et al., 2009). The effects of genetic isolation and the negative qualitative and quantitative effects of ecological traps on isolated populations in natural patches may be additive, or even synergistic, increasing the probability of extinction for those populations. The asymmetric, almost unidirectional, movement across habitats and the functioning of the wheat fields as an ecological trap pose a risk, particularly to small patches that share a long border with the fields relative to their patch area. In such small patches, the loss of individuals that do not reproduce in the patch may be detrimental, due to the reduction in the number of individuals available to replace natural mortality in the patch and due to potentially gradual loss in the quality of the remaining individuals in the patch. We believe that the phenomenon of an ecological trap in agroecosystems is not unique to our study area or to our study species, but may represent an example of a broad phenomenon, probably found in agricultural areas in many places worldwide (see Bollinger et al., 1990; Shochat et al., 2005). Consequently, we think that possible risks of ecological traps should be incorporated in the ‘Wildlife Friendly Agriculture’ approach (see Introduction) that is currently proposed to promote conservation.
Acknowledgements This study was funded by Nekudat Hen foundation. This research was also partially supported by a grant from the Israel Science Foundation (ISF grant 751/09) to Y.Z. We thank our assistants,
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