Oikos 000: 001–011, 2016 doi: 10.1111/oik.03056 © 2016 The Authors. Oikos © 2016 Nordic Society Oikos Subject Editor: Shawn Wilder. Editor-in-Chief: Dries Bonte. Accepted 22 January 2016
Various competitive interactions explain niche separation in crop-dwelling web spiders Itai Opatovsky, Efrat Gavish-Regev, Phyllis G. Weintraub and Yael Lubin I. Opatovsky (
[email protected]), Albert Katz International School for Desert Studies, Blaustein Inst. for Desert Research, Ben-Gurion Univ. of the Negev, IL-84990 Midreshet Ben-Gurion, Israel, and: Regional Agricultural Research and Development Center, Southern Branch (Besor) 85400, Israel. – E. Gavish-Regev, The National Natural History Collections, The Hebrew Univ. of Jerusalem, IL-9190401 Jerusalem, Israel. – P. G. Weintraub, Agricultural Research Organization, Dept of Entomology, IL- 85280 Gilat Research Center, Israel. – Y. Lubin, Mitrani Dept of Desert Ecology, Blaustein Inst. for Desert Research, Ben-Gurion Univ. of the Negev, IL-84990 Midreshet Ben-Gurion, Israel.
Competition for resources is a major organizing principle in communities of organisms that share similar ecological niches. Niche separation by means of exploitation or interference competition was investigated in two taxa of crop-inhabiting spiders that overlap in microhabitat use and have similar web design. Competition for prey and web sites was tested in microcosm experiments with the most common species that build sheet-webs: Enoplognatha gemina (Theridiidae) and Alioranus pastoralis (Linyphiidae). A field survey over the crop season provided data on spatial and temporal dispersion of Enoplognatha spp. (Theridiidae) and linyphiid spiders (Linyphiidae) and on availability of prey over the season. In the microcosm experiments, both taxa took springtails as prey, but only Enoplognatha fed on aphids. Differences in diet, however, could not be attributed to either exploitative or interference competition. Spatial separation of websites was attained by vertical displacement of webs in the vegetation (Enoplognatha) and by avoidance of patches occupied by conspecific or heterospecific individuals (linyphiids). In the field, densities of linyphiids and Enoplognatha were correlated negatively and webs were over-dispersed relative to a random distribution. Both taxa colonized the field at the start of the season; linyphiids colonized as adults, quickly reproduced, and had a second adult peak; Enoplognatha matured in the middle of the season and their numbers remained fairly constant over the season. The combined experimental manipulations and field data suggest that niche separation occurs at different scales. The hypothesis of competition for websites was partially supported, while prey preference (or tolerance) and temporal differences in life history stages also may explain the negative correlations between densities of the two taxa.
Competition for resources is a major organizing principle in communities of organisms that share similar ecological niches. Indeed interspecific competition is often considered responsible for niche partitioning, whereby the realized niches of similar species become more separated in ecological, and sometimes evolutionary, time (Chase and Leibold 2003). Exploitation competition over a resource such as food or foraging sites can lead to a shift in resource use by the weaker competitor, as seen in diet shifts (Abrams 1983, Sih 1993, Bonesi et al. 2004) or the use of an alternative, less preferred habitat (Schoener 1974, Werner and Hall 1977, Gotelli 1997). Interference competition similarly may drive niche separation by directly preventing access to a resource or by controlling a limiting resource through territorial behavior (Schoener 1983). These mechanisms of competition are not necessarily mutually exclusive and several may operate simultaneously (Munday et al. 2001). There is ample theoretical and empirical work supporting the role of interspecific competition in defining the realized niche of many organisms (Chase and Leibold 2003).
Nevertheless, it is frequently difficult to rule out other causes of niche partitioning in ecological time scales. Intraspecific competition (Chesson 2000), apparent competition (Holt 1977), and the occurrence of natural enemies that affect species’ abundances differently (Almany 2004) are other density-dependent processes that can reduce the importance of interspecific competition in determining population persistence. The diverse mechanisms that influence competitive coexistence were summarized by Amarasekare (2002) under three broad categories: competition for resources leading to specialization, temporal partitioning of resources, and spatial partitioning of resources. In addition, densityindependent factors such as availability of refugia and habitat complexity or environmental factors such as seasonal variation or random or episodic disturbance may also reduce competition (Chesson 2000, Liddel 2001, Huisman et al. 2004). In the present study, we examined density-dependent and independent factors affecting niche partitioning in webbuilding spiders along three niche-space axes – resources, space and time.
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As sedentary generalist predators, web-building spiders have long been suggested to have resource-based niche separation, with interspecific competition playing a role in web placement and diet differences among similar species (Wise 1995). Early studies suggested that niche separation is mediated mainly by interspecific interference competition over high quality web sites (Spiller 1984, 1986, Toft 1987). Wise (1995) strongly criticized the interpretation of the results of these studies, and upon re-analysis of data he concluded that there was little, if any, support for the occurrence of interspecific competition in spiders. He suggested instead that densities are usually kept low by other factors (intraspecific competition, predation and densityindependent environmental factors) and do not reach levels where they would be controlled by competition with other species, and therefore such competition will play a minor role in niche partitioning. Some recent studies support this view (Balfour et al. 2003, Birkhofer et al. 2007, Novak et al. 2010). Nevertheless, researchers continued to regard competition as a major cause of niche partitioning in spiders (Herberstein 1998, Harwood and Obrycki 2005), as well as influencing the outcome of other interactions such as invasion success and species replacement (Eichenberger et al. 2009, Houser et al. 2014). Here we revisited the role of interspecific competition for prey and web sites in a seasonal crop habitat that is subjected to recurrent disturbance. Seasonal crop fields are structurally relatively simple and homogeneous environments. However, they undergo episodic disturbance due to crop management, and crop arthropods are subject to periodic extinction and recolonization events (Wissinger 1997). Crops host abundant detritivores and herbivores, potential prey for predators, and many predatory arthropods are known to colonize crops and to take advantage of these resources (Tscharntke et al. 2005, Öberg and Ekbom 2006, Gavish-Regev et al. 2008, Birkhofer et al. 2013). The short growing season favors species of herbivores and their natural enemies that grow rapidly, have short generation times and are good dispersers (Wissinger 1997, Kennedy and Storer 2000). These features could create opportunities for colonizing species to interact frequently and possibly compete over foraging sites and prey. However, as generalist predators, the ability to switch to different prey might reduce competition for food (GavishRegev et al. 2009), and temporal changes in the habitat may enable colonization at different times in the season, reducing competition for websites. Wheat fields in the northern Negev desert of Israel are host to two groups of web-building spiders that overlap in their micro-habitat use and have similar web design and function. Linyphiids and Enoplognatha spp. (Theridiidae) (henceforth, Enoplognatha), build small sheet-webs near the base of wheat plants and in depressions between the plants. The webs trap small flying and jumping insects as well as insects that are dislodged from the wheat plants by wind or by other predators. Using molecular gut-content analysis of field-caught spiders, we found that both of these taxa fed on springtails (Collembola), which are generally common in cereal crops (Chapman et al. 2013), but for Enoplognatha the main prey type was aphids (Hemiptera, Aphidoidea) rather than springtails (Opatovsky et al. 2012). Since most
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aphid species are poor-quality prey, or even toxic in some cases (Toft 2005), we hypothesized that linyphiids compete with Enoplognatha for springtails, causing the latter spiders to shift their diet to the less preferred prey type. A diet shift is one possible means of niche separation in these two web-building spiders, but there exist other possibilities that could operate at different spatial and temporal scales. Webs of both species are individually defended territories and web construction is energetically expensive (Prestwich 1977, Blackledge et al. 2011). If sites for web construction are a limiting resource, spiders might show avoidance behavior, territorial repulsion or intra-guild predation, which would lead to the separation of webs in space (Birkhofer et al. 2007, Gavish-Regev et al. 2009, Welch et al. 2013). The timing of dispersal and colonization of crop fields might be another axis of niche partitioning, giving one species priority over the other in the use of a resource such as suitable web sites or access to refuges. The dominant linyphiid species in the wheat fields, Alioranus pastoralis, is mainly a crop-inhabiting species, but occurs also in nearby desert habitats at the beginning of the crop season (Pluess et al. 2008), while Enoplognatha are found throughout the year mainly in desert habitats (Pluess et al. 2008, Gavish-Regev et al. 2009, Opatovsky unpubl.). Given this distribution, A. pastoralis may have an advantage in being the first to colonize the wheat crop. Enoplognatha adults, however, are larger than A. pastoralis adults, and may be able to displace them from preferred websites (Eichenberger et al. 2009). In the present study, we conducted laboratory experiments to test for the possibility of niche separation along axes of prey or web sites. We simultaneously provided aphids and springtails to paired conspecific and heterospecific spiders. We used the common linyphiid A. pastoralis and the dominant species of Enoplognatha, E. gemina. We first asked if both prey are taken by the two spider species and if one species shifts its diet in the presence of the other, which would support the hypothesis that exploitation or interference competition over prey results in niche separation. As a diet shift could also result from intraspecific interactions, this was tested as well by comparing reduction in number of aphids and springtails by a single spider and by two conspecifics. Second, we tested if there is a spatial separation of web sites on the microhabitat scale by providing individuals with the opportunity to settle near or away from potential competitors and recorded web locations. Using field survey data, we tested whether the abundances of linyphiids and Enoplognatha were correlated over the season at the micro-habitat level. A negative correlation could indicate competition for either prey or web sites. We then asked whether the spatial distributions of spiders and their potential prey were positively correlated, which would indicate the potential for competition over prey. Finally, we examined the patterns of stage-dependent colonization and abundances of the species at the field scale to assess the degree of overlap between adults and juveniles of the species over the crop season. We show that in order to understand the mechanisms underlying niche partitioning in this system, it is essential to consider the species interactions at different spatial and temporal scales.
Material and methods Microcosm experiment I and II: measuring prey reduction and web location Consumption rates of Enoplognatha gemina and Alioranus pastoralis were assessed separately and together with two prey types, an aphid, Schizaphis graminum (Hemiptera, Aphididae) and the springtail Sinella curviseta (Collembola, Entomobryidae). The aphid stock was obtained from fields in the northern Negev and raised in the laboratory on wheat seedlings, while the springtail culture was obtained from the Univ. of Aarhus, Denmark and maintained on baker’s yeast on moistened plaster of Paris. Sinella curviseta is a widespread species found in crops throughout Europe and North America. It was shown to be edible to spiders (Vandomme et al. 2004) and can be raised easily in the laboratory (Draney 2000). Microcosm experiment I
The microcosms were made of soil-filled flowerpots (height 9 cm, radius 11 cm) topped with transparent plastic cylinders (height 20 cm) that were closed at the top with mesh. Wheat seedlings were grown in the microcosm three weeks prior to the experiment and reached a height of 20 cm by the time the experiment started. Adult female A. pastoralis and juvenile Enoplognatha of similar body size, both of which were starved for one week before the experiment, were added to the microcosms according to the following treatments (five replicates per treatment): 1) no spiders (control), 2) one A. pastoralis individual, 3) one E. gemina individual, 4) two A. pastoralis 5) two E. gemina, 6) one individual each of A. pastoralis and E. gemina. The spiders were left in the microcosms for one week in a growth chamber (26°C, 12:12 L:D) to allow web building. On the day of the experiment, 20 springtails and 20 aphids from laboratory colonies were added to each microcosm. After three days, the microcosms were opened and the presence of spiders was noted and the number of aphids and springtails remaining were counted by visually searching the wheat plants and by separating them from the soil using a fine sieve. Microcosm experiment II
The design was similar to the first experiment, with the following differences: 1) we shortened the pre-trial starvation period to reduce the possibility of pre-trial mortality; 2) to increase the opportunity for interactions over prey, fewer prey were added and the experiment duration was longer; 3) we increased the microcosm size (height 15 cm, radius 15 cm; topped with plastic cylinders of height 35 cm) to provide more space for web relocation and 4) the seedlings were grown for four weeks before the experiment started. The spiders were starved for three days before they were added to the microcosms according to the following treatments (six replicates per treatment): 1) no spiders (control), 2) one A. pastoralis individual, 3) one E. gemina individual, 4) two E. gemina individuals, 5) one individual each of A. pastoralis and E. gemina. After four days, ten aphids and ten springtails were added to each microcosm. Ten days after the prey was added, the number of aphids and springtails were counted visually and with a fine sieve to determine
reduction in number of prey, and web height (the distance from web center to the ground) and web diameter were measured. Web size was calculated as the area of a circle. Microcosm experiment III: inter-specific avoidance The experiment was conducted in glass terraria (17.5 ⫻ 40 ⫻ 23 cm) filled with 5 cm of soil. Wheat seedlings were sown in the terraria two weeks prior to the experiment and reached a height of 20 cm by the time the experiment started. Each terrarium (n ⫽ 30 replicates) was divided across the width into two equal parts using a plastic barrier. Two individuals of one species (either E. gemina or A. pastoralis), collected in the field three days before the experiment began, were placed in the same side of the terrarium and were placed in a growth chamber (26°C, 12:12 L:D) to allow web building. After three days the locations of the webs were marked and recorded, the separating barrier was removed and a third individual of the other species was added to the center of the terrarium. After another three days, the web locations of all spiders were noted and web heights were measured to determine if one or both species shifted their webs. Field survey: spider and prey densities The field survey was conducted in an 8.7 hectare wheat field of Kibbutz Be’eri (31°25′37″N, 34°29′34″W), in the northern Negev desert of Israel. The field is surrounded by arid shrubland and planted Eucalyptus trees. In this region, crops are grown year round and therefore the agricultural fields are disturbed frequently. Wheat is seeded in November and harvested for grain in May, and after that fields are left fallow or a summer crop is planted. The wheat field received irrigation in addition to natural winter rains amounting to approximately 250 mm annually, and was not treated with pesticides. Several species of sheet-web building Linyphiidae occur in the wheat fields of the northern Negev (Pluess et al. 2008), but A. pastoralis (female body length 1.91 ⫾ 0.39 mm) was the dominant species during this study. Of the two species of Enoplognatha (Theridiidae) occurring in the fields, E. gemina adults (female body length 3.66 ⫾ 0.65 mm) greatly outnumbered E. macrochelis (female length 3.1–5.2 mm), but juveniles of the two species are indistinguishable in the field and therefore the two species were lumped for the survey data. Spiders and potential arthropod prey were collected in the wheat field on nine sampling dates during the wheat season (December 2010 – May 2011). The sampling was done in 60 quadrats of 0.5m2 each on each sampling date. The quadrats were separated 10 m from one another and from the field edge. They were searched visually and spiders were collected from their webs using a hand-held aspirator, placed in vials, and identified in the laboratory to family, genus, and species when possible, and life stage and sex were recorded. For the analyses, all linyphiid spiders found in sheet-webs were combined under ‘linyphiids’ and all Enoplognatha spp. (Theridiidae) were combined under ‘Enoplognatha’. Spider body length and the height above ground and area of the web were measured for each individual. Potential prey abundance was evaluated using small, web-sized, sticky traps (Harwood EV-3
et al. 2003). In each quadrat, a single sticky trap consisting of a 7.5 cm2 transparent plastic sheet coated on both sides with polybutene trapping adhesive was placed horizontally, 2 cm above ground, to simulate a spider web. The traps were removed after 24 h and the insects were counted and identified to order. Data analysis Microcosm experiments I and II
The reduction in aphid and springtail abundance in the treatment microcosms with one and two spiders was compared to the control microcosms with no spiders with one-way ANOVA or Kruskal–Wallis to determine if the spiders fed on aphids or springtails. In experiment I, treatment means of numbers of prey remaining were compared to the control with a priori least-squares comparisons. In order to test the effect of an additional predator on the predation rate of a potential competitor, we compared the proportion of prey missing to that predicted by the multiplicative predation risk model (Soluk 1993, Sih et al. 1998, Vance-Chalcraft et al. 2004). The null model predicts that if predation is independent, multiple predators will have an additive effect on the probability of predation of shared prey. A non-additive effect can occur due to facilitation of predation of one or more predators, leading to excess prey loss, or to negative interactions among them such as competition or interference, leading to fewer prey lost than expected. The null multiplicative risk model predicts that the proportion of prey lost, for example, to one individual each of E. gemina and A. pastoralis together will be: PEA ⫽ PE ⫹ PA – PE ⫻ PA, where PE ⫹ PA are the additive probabilities of being consumed by a single E. gemina and a single A. pastoralis alone, discounted by PE ⫻ PA, indicating that when prey are consumed by one predator they become unavailable to another predator. To generate the expected values from the null model, the average proportion consumed by one individual of each species was calculated from single spider treatments, and expected values were then calculated for treatments with two individuals of the same species and of the two species together (to test for intra- and interspecific interactions, respectively). The proportion of prey lost in the treatments with two spiders was tested in a twoway ANOVA with predator treatment (two conspecifics and one interspecific) and the categories ‘expected’ and ‘observed’ as factors, in order to test whether the observed predation differed from the expected in each predator combination. A significant difference indicates an interaction effect that could be either synergistic or disruptive. If the interaction is not significant, then the model reduces to an additive model, where the two predators act independently. Finally, web size and height were compared between the two spider species in the different treatments using ANOVA. Microcosm experiment III
Inter-specific avoidance or attraction was tested by comparing the web location of the third spider that was added to the experiment after removing the barrier to the null hypothesis of an equal probability of building on either side using χ2 goodness of fit test. Web heights of E. gemina and EV-4
A. pastoralis were compared in a two-way ANOVA with species and placement order (first or second) as factors. Field survey
The effect of total arthropod density on quadrat occupancy of the two spider taxa (linyphiids and Enoplognatha) was examined using generalized linear model (GLM) with the sampling date as repeated measure. Separately, the effect of the most abundant potential prey group, springtails, on spider density was also tested. Correlations between the densities of the two spider taxa, Enoplognatha and linyphiids, were calculated for each sampling date. Early in the season, spider abundance was very low, and absence of individuals could not be taken as evidence of competition. Thus, plots that had no spider individuals (both Enoplognatha and linyphiids) were not included in the correlations. The dispersion of spiders in the field was calculated using the index of dispersion (I ⫽ mean number of individuals per plot/variance in number of individuals per plot) on each sample date (Krebs 1999). In order to test whether the spiders avoided settling where another individual was already present, a combinatory model was created using MATLAB software (Supplementary material Appendix 1). The model calculated the expected average number of plots colonized by exactly one spider individual, given the number of spiders in the sample, if they were placed randomly into the number of plots available (usually 60 plots at each sampling date, average ⫾ SD 55 ⫾ 9.3). The expected number of plots was compared to the observed number of plots colonized by one individual using χ2 goodness of fit test. ANOVA was used to compare web height and web area by month for the two spider taxa, taking body length into account by regression. In order to determine if presence of another individual in a plot influenced web height and web area, we used GLM with date as repeated measure to compare the average web height of each spider taxon in plots with a single spider and plots with more than one spider. Analyses were performed using Statistica ver.10 (< www. statsoft.com >) and R ver. 3.1.2 (< www.r-project.org >). Data deposition Data available from the Dryad Digital Repository: < http:// dx.doi.org/10.5061/dryad.k2d8t > (Opatovsky et al. 2016).
Results Microcosm experiment I and II: prey reduction and web height In all microcosm experiments aphids, being parthenogenetic and viviparous, reproduced in the microcosms, but springtails did not reproduce during the experiments. In microcosm experiment I, the overall effect of treatment on the number of insects remaining was significant for springtails but not for aphids (springtails: F5,24 ⫽ 3.93, p ⫽ 0.01, Fig. 1A; aphids: F5,24 ⫽ 1.47, p ⫽ 0.22; Fig. 1B). A single Alioranus pastoralis reduced the number of springtails relative to the control (Fig. 1A; t ⫽ 12.95, p ⫽ 0.001) and a single
Figure 1. Microcosm experiments I and II. The average (⫾ SE) number of prey individuals remaining at the end of the experiment. Experiment I (A, B) and experiment II (C, D). Bars represent the average number of springtails (A, C) and aphids (B, D) ⫾ SE remaining at the end of the experiment. Experiment I treatments (n ⫽ five replicates each): 1) no spiders (control), 2) one individual of A. pastoralis (Ap), 3) one individual of E. gemina (Eg), 4) two individuals of A. pastoralis (Ap⫹ Ap), 5) two individuals of E. gemina (Eg⫹ Eg), 6) one individual of A. pastoralis and one individual of E. gemina (Ap⫹ Eg). Experiment II treatments (n ⫽ six replicates each): 1) no spiders (control), 2) one individual of A. pastoralis (Ap), 3) one individual of E. gemina (Eg), 4) two individuals of E. gemina (Eg⫹ Eg), 5) one A. pastoralis and one E. gemina. The asterisks indicate significant (p ⬍ 0.05) a priori comparisons.
Enoplognatha gemina reduced the number of aphids relative to the control (Fig. 1B; t ⫽ 4.3, p ⫽ 0.04). However, when two spiders of the same or different species were present, the numbers of springtails and aphids remaining at the end of the experiment did not differ from the control (Fig. 1A–B, p ⬎ 0.05 for all). In experiment I, the observed proportion of prey consumed in the treatments with two spiders differed significantly from expected from the multiplicative model with both aphids and springtails as prey (two-way ANOVA, F1,34 ⫽ 6.6, p ⫽ 0.01 and F1,34 ⫽ 5.1, p ⫽ 0.03, respectively). The proportion of prey consumed was lower than expected, indicating non-additivity (Fig. 2). However, the interaction between the factor “observed versus expected” and the treatments (two conspecific pairs or the heterospecific pair) was not significant, indicating that in the microcosms with A. pastoralis and E. gemina the proportion of aphids or springtails consumed did not differ from those with two conspecifics of either species (aphids, F2,34 ⫽ 1.6, p ⫽ 0.22; springtails, F1,34 ⫽ 0.55, p ⫽ 0.58). In microcosm experiment II both springtail and aphid numbers were lower in the treatment microcosms relative
to the control (Fig. 1C–D), however the effect of treatment on the proportions of prey remaining was significant only for springtails (Kruskal–Wallis, springtails: H4,30 ⫽ 13.4, p ⫽ 0.01; aphids: H4,30 ⫽ 8.87, p ⫽ 0.06). After 10 days, the number of aphids in the control microcosms had increased by two orders of magnitude due to reproduction and the variance was very high, likely masking the effect of predation. The proportion of prey consumed in the treatments with two individuals of E. gemina and one E. gemina plus one A. pastoralis was significantly different from the predictions from the multiplicative model for aphids (F1,20 ⫽ 4.8, p ⫽ 0.04), but not for springtails (F1,20 ⫽ 2.51, p ⫽ 0.13). However, as in experiment I, there were no significant interactions, indicating that there were no differences in the reduction of prey between the heterospecific and conspecific treatments. Survival of A. pastoralis in the experiment was low (two survived out of six when alone), but did not differ with E. gemina present (one survived out of six). Enoplognatha gemina survival was also not influenced by the presence of competitors of either species (all six survived when alone; five survived out of six with A. pastoralis, and five survived EV-5
Figure 2. Microcosm experiment I. Average (⫾ SE) observed (black columns) and expected (white columns) proportions of springtails (A) and aphids (B) eaten in treatment with two spiders (two individuals of A. pastoralis – Ap⫹ Ap, two individuals of E. gemina – Eg⫹ Eg, one individual of A. pastoralis and one individual of E. gemina – Ap⫹ Eg. Expected proportions were calculated from the multiplicative model (PEA ⫽ PE ⫹ PA – PE ⫻ PA).
out of six with another E. gemina). Intra-guild predation was not observed. Webs of A. pastoralis were smaller than those of E. gemina (F4,32 ⫽ 8.28, p ⫽ 0.003, post hoc comparisons between A. pastoralis and E. gemina were all p ⬍ 0.05, Fig. 3), but neither spider species changed its web area when a potential competitor was present. Alioranus pastoralis webs were constructed lower on the wheat stem than those of E. gemina and the web height of A. pastoralis did not change in the presence of another individual. The height of E. gemina webs, however, increased in the presence of another individual of either species (F2,15 ⫽ 20.69, p ⬍ 0.0001, post hoc comparisons between A. pastoralis and E. gemina and the average of two E. gemina in all treatments were p ⬍ 0.05, Fig. 3). In the treatment with two E. gemina individuals one individual increased it web height (higher web 10.6 ⫾ 8.6 cm and lower web 3 ⫾ 1.5 cm; average ⫾ SD) but the difference was not significant (W ⫽ 10, p ⫽ 0.1, Wilcoxon signed rank test).
Figure 3. Microcosm experiment II. Web area (cm2, white bars) and web height above ground (cm, black bars) of A. pastoralis (Ap) when alone or with E. gemina (⫹ Eg); and of E. gemina (Eg) when alone, with A. pastoralis (⫹ Ap) and with another E. gemina individual (⫹ Eg). The error bars represent 1 SE The letters above the bars show significant differences (p ⬍ 0.05): capital letters are comparisons of web area and lower case letters indicate web height comparisons.
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Microcosm experiment III: inter-specific avoidance Alioranus pastoralis built their webs more often on the side of the terrarium without potential competitors of either species: 24 out of 30 individuals built on the unoccupied side (χ2 ⫽ 6.53, p ⫽ 0.01, n ⫽ 30), while E. gemina built webs indiscriminately on both sides of the terrarium: 13 out of 30 individuals built on the unoccupied side (χ2 ⫽ 2.61, p ⫽ 0.1, n ⫽ 30). The webs of E. gemina were located higher than those of A. pastoralis, whether they were built first or added after A. pastoralis (E. gemina web height – placed first: 1.94 ⫾ 0.79 cm, placed second: 2.1 ⫾ 0.78 cm; A. pastoralis web height – placed first: 1.35 ⫾ 1.35 cm, placed second: 1.16 ⫾ 0.95 cm, average ⫾ SD; species: F112 ⫽ 14.56, p ⫽ 0.0002; placement order: F112 ⫽ 0.01, p ⫽ 0.98; species ⫻ placement order: F112 ⫽ 0.71, p ⫽ 0.4). Field survey: spider and prey densities In total, 160 individual Enoplognatha and 229 linyphiids were collected from their webs in the field plots during the crop season (maximum of seven individuals per plot and average of 0.6 ⫾ 1.04 individuals per plot; average ⫾ SD). Both taxa were present in the wheat field throughout the season (December–May), but their abundances and development stages differed over the season. Juvenile Enoplognatha dispersed into the wheat field at the beginning of the season and were present throughout the crop season. Sub-adults peaked in January–February and adults in February–March (Fig. 4A), thus the juveniles present in the second half of the season could be either additional migrants or the result of local reproduction. Linyphiids first appeared as adults at the beginning of the season and completed one full life cycle within the field (Fig. 4B). The first adult peak occurred in January, overlapping with sub-adult and juvenile Enoplognatha and a second, larger one in March when only juvenile Enoplognatha were present in the field. Potential prey abundance increased until March and then decreased until the end of the crop season (Fig. 4). Consequently, for some analyses we divided the crop season
Figure 4. Densities (average number per m2) of Enoplognatha (A) and linyphiids (B), and the abundance of potential prey in quadrats in a wheat field over the crop season. The vertical dotted line separates early and late periods in the cropping season, corresponding to periods of increasing and decreasing prey abundance, respectively. The solid black line represents adult spiders, the dotted black line represents juveniles and sub-adults, and the solid grey line represents potential prey captured on the sticky traps.
into the two periods reflecting the increasing and decreasing abundance of potential prey, respectively. The lowest arthropod abundance was two individuals per sticky trap per day, while the highest was over 60 per trap; average ⫾ SD 10.5 ⫾ 14.0). Springtails constituted 11 to 83% (average ⫾ SD 50 ⫾ 34.5%) of the total arthropods over the season. There was no significant effect of total prey abundance or of springtail abundance alone on spider abundances in the plot (total prey: linyphiids R2 ⫽ 0.005, F1,216 ⫽ 0.15, p ⫽ 0.69, Enoplognatha R2 ⫽ 0.001, F1,216 ⫽ 0.05, p ⫽ 0.83; springtails: linyphiids R2 ⫽ 0.03, F1,216 ⫽ 2.3, p ⫽ 0.13, Enoplognatha R2 ⫽ 0.01, F1,216 ⫽ 0.05, p ⫽ 0.83). Abundances of linyphiids and Enoplognatha were negatively correlated throughout the season, and significantly so for the first period of the wheat season (Fig. 5A). Indices of dispersion ranged from 0.93 to 2.04; in all months except February (I ⫽ 0.83, p ⫽ 0.01), spider distribution was dispersed when compared to a Poisson distribution (p ⬎ 0.1).
In all but two sampling dates, spiders were found alone in a greater proportion of the plots than expected based on the probability model (p ⱕ 0.05) (Fig. 5B). We compared spider size (body length), web height above ground and web area between the two taxa over the sampling months. As only a single Enoplognatha individual was measured in April, this month was excluded from the analyses. There were significant differences in spider size over the sampling months (F4,292 ⫽ 25.82, p ⬍ 0.0001) and there was a significant interaction between taxon and sampling month (F4,292 ⫽ 5.065, p ⫽ 0.0006): Enoplognatha individuals were 1.3–1.5 times larger than A. pastoralis in all months except May when there were no adult Enoplognatha (Fig. 6A). Web height and web area were significantly positively correlated for both taxa (Enoplognatha: r ⫽ 0.27, p ⬍ 0.05, linyphiids: r ⫽ 0.39, p ⬍ 0.05), but neither was correlated with spider body length (p ⬎ 0.05). Web height varied over the sampling months (F4,292 ⫽ 5.84, p ⫽ 0.0002),
Figure 5. (A) Correlations between linyphiid and Enoplognatha densities on each of the sampling dates. Circles are correlation coefficients; filled circles are statistically significant (p ⬍ 0.05) coefficients. (B) Proportion of plots that were colonized by a single spider (solid black line), two or more conspecifics (dotted black line) or two or more heterospecifics (solid grey line). The asterisks represent dates on which the number of plots with one individual was significantly greater than expected based on a random distribution.
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Figure 6. (A) Average spider body length (mm) and (B) web area (cm2) of Enoplognatha (grey line) and linyphiids (black line). The error bars represent the standard errors. The vertical dotted line separates the early and late periods in the crop season (Fig. 4).
with Enoplognatha webs placed slightly higher in the vegetation than those of linyphiids in all months except March (Fig. 6B). However, there was no significant difference in web height between the two taxa and the interaction between taxon and sampling month was significant (F4,292 ⫽ 2.88, p ⫽ 0.023). There were no effects of sampling month or taxon on web area (p ⬎ 0.05 for both). We compared web area and height in plots when a spider was alone and with other spiders. The presence of another spider of either taxon had no effect on these two measures (web height: linyphiids F1,114 ⫽ 0.73, p ⫽ 0.11, Enolopgnatha F1,102 ⫽ 0.26, p ⫽ 0.78; web area: linyphiids F1,114 ⫽ 0.16, p ⫽ 0.87, Enolopgnatha F1,102 ⫽ 0.12, p ⫽ 0.90).
Discussion We investigated prey preference and spatial and temporal separation as possible mechanisms of niche separation in two groups of web-building spiders occupying the same microhabitat, namely soil depressions and stems at the base of wheat plants. In laboratory microcosm experiments, we confirmed that Enoplognatha gemina consumed aphids while Alioranus pastoralis did not. Yet they shared a common prey, springtails, one of the most abundant potential prey types in the wheat fields. In the microcosm experiments, E. gemina webs were placed higher on the wheat plant and the spiders moved their webs up in the presence of either a conspecific or A. pastoralis. Alioranus pastoralis, by contrast, showed horizontal displacement in the presence of E. gemina. In the wheat field, we found no relationship between the distribution of Enoplognatha or linyphiids and that of potential prey. Web height on the wheat plants did not differ in the field, but spiders of both taxa were overdispersed in the field, particularly in the first half of the wheat season when Enoplognatha were most abundant and numbers of potential prey were increasing. Separation by prey preference initially seemed a likely hypothesis, as DNA analyses of gut contents indicated that Enoplognatha spp. feed on aphids while linyphiids do not (Opatovsky et al. 2012). In microcosm experiment I,
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only E. gemina significantly reduced the number of aphids after 3 days. This was not seen, however, in experiment II, where after 10 days aphid numbers had increased more than 10-fold due to reproduction. Gavish-Regev et al. (2009) estimated that an adult E. gemina consumed 3–4 aphids over 48 h, or a maximum of 2 per day. Thus, over 10 days any decrease in number of aphids due to predation by one or two spiders would scarcely be noticed. In laboratory experiments (Al-Beiruti 2013), starved A. pastoralis attacked the aphid Sitobion avenae when it was offered as the sole prey type, but the spiders lost weight when attempting to feed on them. Enoplognatha gemina, by contrast, attacked S. avenae and gained weight feeding on them. Thus, the difference in the diet observed in E. gemina and A. pastoralis is likely due to intrinsic differences in their ability to utilize aphids as prey, rather than a diet shift in Enoplognatha driven by competition. The unpalatability of many aphid species (Toft 2005, Schmidt et al. 2013) suggests that aphid-feeding is an evolved specialization occurring in relatively few predator species (see also Sloggett and Davis 2010). On an evolutionary time scale, specialization on a low-quality prey type may result from competition, which would then lead to niche separation and speciation (Connell 1980). This mechanism requires the evolution of morphological or physiological adaptations of the predator and constant and sufficiently high abundance of the prey, and it usually leads to lower fitness when utilizing other prey types (Rana et al. 2002). While some epigeal spiders consume aphids even when their abundance is low (Chapman et al. 2013), it remains unknown whether Enoplognatha requires aphids and whether it has specific adaptations for feeding on them. The microcosm experiments showed that both A. pastoralis and E. gemina fed on springtails and significantly reduced their abundance relative to control microcosms. Using the multiplicative risk model (Sih et al. 1998) we found that both conspecific and interspecific pairs of spiders showed no additive effect on springtail consumption and did not differ from one another. Such non-additivity could result from intraguild predation or from interference between the two predators, both of which would lower the rate of prey consumption (Ferguson and Stiling 1996, Lang 2003,
Snyder and Ives 2003). Intra- or interspecific predation was not observed in the experiments. Alioranus pastoralis had high mortality over the 10 days of experiment II, yet the mortality rate was high in both treatments with a single spider and two spiders, suggesting that it was not due to intraguild predation, but rather to an unknown cause. The case for interference competition for space is strengthened by two observations: one of the E. gemina individuals shifted its web upward on the wheat plant in the presence of another individual (experiments II and III) and A. pastoralis shifted away from E. gemina when provided with space to move horizontally (experiment III). Interference competition is known to affect the distribution and use of foraging sites in spiders (Schmidt and Rypstra 2010, Schmidt et al. 2013) and in other trap-building predators (Scharf et al. 2010). In the field survey, body size, web height and web area varied with season, but the two taxa did not differ significantly in any of these measures. Based on the microcosm experiment results, we expected that webs of Enoplognatha would be placed higher than those of linyphiids. While this was the trend over most of the season, the difference was not significant; furthermore, web height was unrelated to spider density. The lack of evidence for vertical separation in the field surveys was surprising. However, field densities of these web-building species were generally low throughout the season and vertical separation of webs might only occur at higher spider densities (as in the microcosm experiments). Alternatively, the choice of web height in the vegetation might be related to foraging decisions rather than to intra- or inter-specific interactions. For example, in laboratory experiments, the aphid-feeding linyphiid Mermessus denticulatus increased its web height on wheat plants when aphids were available as prey (Gavish-Regev et al. 2009) and the linyphiid Grammonota inornata changed the web structure according to prey availability (Welch et al. 2013). In our study site, aphid densities were low and springtails were available throughout the season, such that shifts in foraging sites may not have been necessary. Other potential influences on web placement and foraging sites, such as predation risk and cover (Schmidt and Rypstra 2010, Schmidt et al. 2014), were not investigated here. Both Enoplognatha spp. and linyphiids tended to settle alone in plots more often than expected by chance, and their abundances were negatively correlated. The densities of the two taxa were unrelated to prey densities and thus prey availability does not appear to be a major determinant of this pattern of dispersion. Nonetheless, competitive displacement occurred in the microcosms and may partially explain the field data. The apparent avoidance of both conspecifics and heterospecifics was pronounced in the first half of the wheat season, when population density was increasing in both taxa. While space for actual web construction may not be limiting at average field densities of two spiders per m2, over-dispersion could be caused by encounters among dispersing individuals at the stage when they are searching for suitable web sites. Spiders produce a dragline while walking or bridging and the presence of draglines left by other searching spiders may cause an individual to reject a potential web site (Persons et al. 2001). In addition, some linyphiids (in particular Erigoninae, e.g. Alioranus;
Alderweireldt 1994) are known to search for prey off their webs and thus may occupy an area larger than the actual capture web. There was no clear pattern of dominance in the field. Juvenile Enoplognatha and adult linyphiids both colonized the wheat fields at the beginning of the season. Linyphiid adults were able to reproduce immediately resulting in a second peak in mid-season, while Enoplognatha matured only at mid-season. Consequently, by March, linyphiid density in the plots was 2–3 times that of Enoplognatha, having increased from an average of 1 per m2 to about 6 per m2. Linyphiid species occurring in wheat fields are cropadapted spiders with short life cycles that are able to build up high population densities over the short cropping season (Gavish-Regev et al. 2008, Birkhofer et al. 2013). In northern Negev wheat fields, colonizing linyphiids arrive from other crops (Opatovsky unpubl.) or possibly from resident populations that survive the inter-crop period (Gavish-Regev et al. 2008, Opatovsky and Lubin 2010) and quickly become abundant in the fields (Gavish-Regev et al. 2008, this study). Enoplognatha are desert spiders occurring typically in low densities in the arid habitat surrounding the crop fields, but able to disperse aerially (ballooning on silk) into crop fields throughout the season (Gavish-Regev et al. 2008, Pluess et al. 2008). A relevant model for species interactions and coexistence in such systems may be a colonization–competition tradeoff (Calcagno et al. 2006). The extinction and re-colonization cycles typical of seasonal crops together with their low spatial heterogeneity are expected to disfavor high predator abundance (Langellotto and Denno 2004). Yet, many species are opportunistically good colonizers and are able to take advantage of such temporarily prey-rich habitats (Birkhofer et al. 2013), and more than one mechanism is likely responsible for the diversity and abundance of predators in crop fields (Lensing and Wise 2004, Clough et al. 2005, Batáry et al. 2008, Schmidt and Rypstra 2010). Both linyphiids and Enoplognatha are typically colonizers of disturbed habitats. While the crop-inhabiting linyphiids have a reproductive advantage, Enoplognatha may have a competitive advantage due to their size at least during part of the life cycle in the crop. While they are slow to mature, they are able to do so utilizing a wider variety of prey types (including aphids) than the linyphiids (see also Opatovsky et al. 2012) and as adults they may displace the smaller linyphiids, a possibility that was not tested here. In summary, the combined field and experimental data suggest that at high densities interference competition between linyphiids and Enoplognatha spp. might lead to vertical stratification of webs. However, at the typical field densities that we observed, direct intraspecific and interspecific competition is likely avoided by individuals spacing themselves widely. While the timing of colonization overlapped broadly, the divergence in body sizes later in the season and the ability of Enoplognatha spp. to feed on aphids as well as springtails could contribute to niche separation among the two taxa. Thus, our study only partially supports Wise’s argument that inter-specific competition under field conditions is a weak force and may not be responsible for niche partitioning (Wise 1995).
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By investigating interactions occurring at different spatial and temporal scales, we are better able to explain the mechanisms underlying coexistence of potentially competing species. A combination of experiments and field survey data is essential to arrive at an understanding of the dynamics of these interactions. Some open questions remain regarding, for example, the importance of interference competition at the field scale, which might be investigated by experimental manipulation of spider densities in the field. Predation pressure and refuge availability are difficult to study in the field, but can be investigated experimentally. More field data would be necessary to establish whether a competition– colonization tradeoff exists in such systems. Finally, we may ask whether intraguild interactions influence the potential of these spiders to suppress pest populations in crop fields (Snyder and Wise 1999) and whether arid-habitat species such as Enoplognatha play a more important role in aphid suppression in spite of their lower densities than typical agricultural species such as linyphiids. Acknowledgements – We thank Z. Heker (Kibutz Be’eri) for the use of their fields and D. Perlstein for assisting with the mathematical model. We thank also I. Giladi, M. Segoli and J. Rosenheim for providing valuable comments on an earlier version of this manuscript. The study was supported by research grants from Ministry of Agriculture (857-0578-09) to YL and the JNF (Emilio Sacerdote fund, 02-4682), Sigma Xi grant-in-aid of research and Kreitman postdoctoral scholarship (Ben-Gurion University) to IO. This is publication no. 898 of the Mitrani Dept of Desert Ecology.
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Supplementary material (available online as Appendix oik-03056 at < www.oikosjournal.org/appendix/oik-03056 >). Appendix 1.
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