Mountains imply enormous environmental variation, with alpine habitats entailing harsh environ- ments, especially for ectotherms such as lizards. This environmental variability also may imply variation in prey availability. However, little is known about how lizard trophic ecology varies with elevation. In this study, we analyze diet, prey availability, prey selection, and trophic niche width in the lacertid lizard Psammodromus algirus along a 2,200-m elevational gradient in the Sierra Nevada (SE Spain). The analysis of fecal samples has shown that Orthoptera, Formicidae, Hemiptera, Coleoptera, and Araneae are the main prey, although, according to their abundance in pitfall traps, Formicidae and Coleoptera are rejected by the lizard whereas Orthoptera, Hemiptera, and Araneae are preferred. Prey abundance and diversity increase with elevation and diet subtly varies along with the elevational gradient. The consumption of Coleoptera increases with elevation probably as a consequence of the lizard foraging more in open areas while basking. The electivity for Araneae increases with elevation. Araneae are rejected in the lowlands—where they are rela- tively abundant—whereas, at high elevation, this lizard positively selects them, despite they being less abundant. The lizard trophic niche width expands with elevation due to concomitant greater prey diversity and hence this lizard feeds on more prey types in highlands. Although no sex differ- ence in diet has been found, the trophic niche is broader in females than males. As a whole, alpine lizards show a trophic niche similar to that found at lower elevations, suggesting that P. algirus is well adapted to the harsh environment found in alpine areas. Key words: alpine habitats, arthropods, mountain ecology, niche variation hypothesis, trophic ecology High mountains present harsh environmental conditions for life, such adapted to the conditions of each elevation (Keller et al. 2013). If local as low temperatures, high solar radiation, and low oxygen pressure adaptation is insufficient, as these species move away from their opti- (Ko ¨rner 2007). Consequently, diversity is usually lower in alpine mal habitat, their fitness drops, being minimal in marginal habitats zones in comparison with mid- and lowlands (Nogue ´ s-Bravo et al. such as alpine environments (Kawecki 2008). 2008). However, widespread species may occur along the elevational Trophic ecology is fundamental to understand ecosystem func- gradient in mountains, embracing different environmental conditions. tioning and relationships among species (The ´ bault and Fontaine In such cases, species broadly distributed over an elevational gradient 2010), as well as the evolution of several life-history traits (Edwards typically show phenotypic divergence, with populations locally et al. 2013). An optimal diet (in quality as well as in quantity) is V C The Author(s) (2017). Published by Oxford University Press. 603 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 604 Current Zoology, 2018, Vol. 64, No. 5 fundamental to maximize fitness (Franzke and Reinhold 2012; elevations, and in prey found under shrubs at lowlands. Lefcheck et al. 2013; Nel et al. 2015). It also affects aspects as rele- Moreover, we predict a greater proportion of highly chitinous vant as the immune system or sexually selected traits (Schlotz et al. species in the diet with elevation, since lizards are larger at high 2013; Brunner et al. 2014; Kopena et al. 2014). In this sense, little altitudes (Zamora-Camacho et al. 2014a), and hence they may information is available on how the diet of widespread species varies subdue harder prey. with elevation. If animals are locally adapted along the elevational 2. We determine how the trophic niche width of this lizard varies gradient, their diet is expected to be optimal along it. However, if with elevation, with special emphasis in the alpine zone. We pre- some habitat—particularly the alpine area—is suboptimal for the dict that diet may diversify with elevation as a consequence of dif- species, diet may be impoverished. A narrower trophic niche may ferent factors such as reduced interspeciﬁc competition (Comas imply fewer nutrients, which may translate as lower consumer fit- et al. 2014), increased body size with elevation (Zamora- ness (Pulliam 1975; Raubenheimer and Simpson 1997; Lefcheck Camacho et al. 2014a), or increased prey diversity. We test the et al. 2013). niche variation hypothesis by comparing the elevational variation Diet may change with elevation as a consequence of different in population diet width with the mean of individual diet width of factors, such as variation in microhabitat use or in prey availability. lizards. If population diet diversiﬁes as a result of greater individ- For example, with elevation, ectotherms should spend more time ual diet diversity for each lizard, a positive correlation between basking in open areas (Dı ´az 1997), where available prey may differ population diet width and individual diet width is predicted. from those found near their shelters (Belliure et al. 1996). As a con- However, if population diet width augments due to a greater sequence of a reduced activity period with elevation, animals may diversity of specialized individuals, no correlation between popu- vary their foraging mode, being more selective and preying on more lation diet width and that of the individual is expected. profitable species (Perry 2007). Moreover, if morphological or phys- 3. We test for sex differences in diet and diet width. Males are iological changes are associated with elevation, we can expect asso- more mobile while defending their territories and searching for ciated changes in their diet. For example, if animals vary in speed or mates (Dı ´az 1993), implying a higher rate of encounters with other ability to catch, subdue, or handle prey, concomitant changes different prey types. Males are also quicker (Zamora-Camacho in the percentage of highly evasive prey are expected (Miles et al. et al. 2014b), which would favor the capture of a more diverse 2007). For instance, populations with larger specimens may show a array of prey (sedentary as well as evasive). They also have diet richer in larger and more chitinous species. larger heads (Mellado and Martı ´nez 1974), favoring the capture Moreover, ecosystem conditions could influence dietary varia- of more diverse prey in hardness and size. Accordingly, we pre- tion with elevation. On the one hand, lower diversity with higher dict that males will show a wider diet and will consume more elevation may imply fewer competitors, allowing a niche release evasive and harder species than do females. (Pianka 1994), and hence an increase of the niche width with eleva- tion (Comas et al. 2014; also see Costa et al. 2008a). On the other Materials and Methods hand, if the decreased diversity also applies to prey, then niche width may narrow with elevation. Whatever the pattern with elevation, Study species greater total niche width at the population level may result from Psammodromus algirus is a medium-sized lizard (60–90 mm adult 2 different mechanisms: more variety of trophic specialist individu- snout–vent length, SVL) distributed in south-western Europe and als (the niche variation hypothesis, Van Valen 1965; Bolnick et al. north-western Africa, where it inhabits shrubby habitats (Dı ´az and 2007), or every individual being more generalist (Bearhop and Carrascal 1991). In SE Spain, it occurs along an elevational gradient Adams 2004). At the same time, if body size varies along the gra- from sea level to more than 2.600 m.a.s.l. (Ferna ´ ndez-Cardenete dient, populations with larger animals might show a greater diet et al. 2000). This lizard typically searches actively for its prey width as a result of the higher diversity of the prey being consumed (Belliure et al. 1996). Its diet is very broad, composed mainly of (Dı ´az 1994b). arthropods such as Araneae, Formicidae, Coleoptera, Hemiptera, In this regard, lizards can be used as model organisms, because Orthoptera, and Diptera (review in Salvador 2015). they play an important role in ecosystems as generalist predators (Huey and Pianka 1981; Huey et al. 1983; Reilly et al. 2007). In par- Study area ticular, lacertids, the dominant group of lizards in Mediterranean The study area was located in the Sierra Nevada mountain (SE ecosystems, perform an essential role as a vehicle of matter and 0 00 0 00 0 00 0 00 Spain, 2 56 1 2–3 38 02 2 W and 36 56 10 0–37 12 58 9 N). Six energy from invertebrates to birds and mammals (Valverde 1967). sampling plots were established along the elevational gradient, sepa- Accordingly, in the present study, we analyze the variation in diet, rated by roughly 500 m of elevation: 300, 700, 1,200, 1,700, 2,200, prey availability, prey selection, and trophic niche width of the liz- and 2,500 masl (Figure 1). Sampling was carried out consistently ard Psammodromus algirus along an elevational gradient of within the typical habitat of P. algirus: areas with abundant herbs 2,200 m in the Sierra Nevada (SE Spain). With the aim of character- and shrubs ranging from 40 to 100 cm high and relatively high vege- izing the diet of this lizard, we undertake the following: tation cover (Dı ´az and Carrascal 1991). Care was taken selecting locations with similar habitat structure despite the variation in plant 1. We examine the elevational variation in diet and analyze how communities along the elevational gradient. For more details on the prey availability and prey selection vary with elevation. We pre- study area, see Zamora-Camacho et al. (2013, 2016). dict that diet will change with elevation according to several fac- tors such as variation in prey availability, the lizard’s use of Diet analysis microhabitat, and body size of the lizards. For this species, con- sidering how its basking behavior varies with elevation (Belliure Fecal samples (pellets) were used for diet analysis, this information et al. 1996; Dı ´az 1997; Zamora-Camacho et al. 2016), we pre- on lizards’ diet being as reliable as stomach contents (Garrido et al. dict the diet to be richer in species found in open areas at high 2011) and allowing us to keep individuals alive. As a part of a Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Moreno-Rueda et al. Prey availability and selection in Psammodromus algirus 605 Figure 1. Location of the Sierra Nevada mountain in Spain, and location of the 6 sampling points, where the study was performed, in a 3-dimensional map. Numbers indicate the location of sampling points at 300 masl (1), 700 masl (2), 1,200 masl (3), 1,700 masl (4), 2,200 masl (5), and 2500 masl (6). long-term study between 2010 and 2012, we regularly captured liz- and relative abundance as the percentage of a prey item in relation ards along the elevational gradient. When lizards deposited feces to the total number of prey items (% of frequency). We also deter- just after being captured (hence, being ensured that fecal content mined the number of prey per pellet. Trophic niche width was esti- was from the diet of the animal in the field), we kept feces in labeled mated using the B Levins’ index (Simpson 1949; Levins 1968), in its vials with ethanol (96%). Only pellets from adult individuals were standardized version Bs (Hurlbert 1978): considered. Adults were recognized as those reaching a minimum B ¼ ; SVL (measured with a ruler, 0.1 mm of accuracy) for each sex and Rp each elevation (according to Reguera et al. 2014). Sex was deter- mined by secondary sex characters, mainly femoral pores, which are B 1 more developed in males (Iraeta et al. 2011). Pellets were examined Bs ¼ n 1; in the laboratory through a 10–40 binocular dissecting micro- scope, and items were identified to the lowest taxonomical level pos- where p is the fraction of items in the diet that are of food sible. Identification was based on non-digestible remaining category j, and n is the number of possible food categories fragments such as cephalic capsulae, jaws, thoraxes, etc. Then, we (Krebs 1999). Bs ranges from 0 (100% utilization of a single food assigned the items to operational taxonomic units (OTUs, Sneath category) to 1 (equal use of all categories). Levins’ index was and Sokal 1962), usually at the level of Order, except for the estimated as a whole and for each sex and elevation. Moreover, Formicidae family, which was separated from other Hymenoptera we estimated the individual trophic niche width (Bi) for each because of their particular morphological and ecological characteris- lizard, considering the prey found in individualized pellets. tics, and for larvae, usually included in the same OTU. Moreover, It should be noted that, while Bs indicates the trophic width niche OTUs were assigned to categories of evasiveness and hardness (in at the population level, Bi indicates the trophic width niche at both cases: low, medium, and high) according to criterion in Table the individual level. The trophic niche overlaps between sexes 14.1 in Vanhooydonck et al. (2007). (m and f corresponding to males and females) with resource For each prey type, we calculated relative occurrence as the utilization p and p , was calculated by Pianka’s index (O ) mi fi mf percentage of individuals consuming that prey type (% of presence), (Pianka 1974): Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 606 Current Zoology, 2018, Vol. 64, No. 5 R p p mi i¼1 fi O ¼ O ¼ qﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃ : mf fm 2 2 R ðÞ p ðÞ p mi i¼1 fi To make an elevational comparison, we had to use similar sam- ple sizes along the elevational gradient. If some sampling points had larger sample sizes than others, prey species rarely consumed would be easier to detect, the number of OTUs could be larger, and trophic niche width would appear greater. To avoid this bias, we used only 12 fecal samples per elevation, 6 from males and 6 from females. A rarefaction curve showed that 12 samples were sufficient to attain 75% of the whole diversity of OTUs, and increasing the number of OTUs recorded to up 90% would require twice this sample size (Figure 2). However, we had collected a large quantity of feces (n ¼ 65; 35 from males and 30 from females) for the alpine zone Figure 2. Curve of rarefaction showing the rate at which new OTUs are incor- (2,200 and 2,500 masl). Given that this was the elevational limit for porated as sample size increases, from a randomly selected sample. this species (Ferna ´ ndez-Cardenete et al. 2000), we considered that more detailed knowledge of the diet in the alpine zone would be use- we used the Spearman rank binary correlation (q) in order to test a ful, and hence added a separate analysis restricted to this area. relationship between the elevation (considered here as a continuous variable) and the dependent variable to test. The data were trans- Prey availability formed when necessary in order to fulfil the criterion for normality To estimate the availability of potential prey for P. algirus, during and homoscedasticity. All the analyses were performed with 2010, we installed 30 pitfall traps in each location along the eleva- Statistica 8.0 (StatSoft 2007) following Quinn and Keough (2002). tional gradient (Woodcock 2005). Given that this species is an opportunistic active forager, we tried to cover the whole range of foraging places, dividing sampling areas into 2 micro-habitats: open Results areas (basking sites) and under shrubs (shelter sites), with 15 traps Diet of P. algirus along the elevational gradient in each, a minimum of 5 m apart to safeguard the independence of In the analysis comparing the points along the elevational gradient, the data (Ward et al. 2001). Traps remained open from early morn- overall, we found 456 prey of 15 different OTUs (n ¼ 72 individuals; ing until dusk, once every 2 weeks, entirely coinciding with the Table 1). The main preys (those with frequencies over 10%) were activity period of the lizards for each elevation (Zamora-Camacho Orthoptera, Formicidae, Coleoptera, and Hemiptera (Table 1). et al. 2013). At sundown, trap content was individually collected in Moreover, Orthoptera was notable for being present in 79% of the labeled vials and preserved with ethanol (96%). In this way, we cap- feces samples, and Araneae were found in more than a half of the tured only arthropods that could have been potentially consumed by samples (54%; Table 1), hence these prey types were widely con- this diurnal lizard. Pitfall traps may underestimate some groups such sumed. Considering only the 5 most frequent OTUs in the diet of as sedentary prey, flying insects, or Orthoptera, and therefore, the P. algirus (Orthoptera, Formicidae, Coleoptera, Hemiptera, and findings must be interpreted taking into account that the availability Araneae), there were no significant differences in the consumption of these groups may be underestimated. Each prey was identified in frequency between males and females (Table 2). The overlap the laboratory under a 10–40 binocular microscope and assigned between sexes for each elevation was tight, that is, between 0.60 to an OTU, using the same criteria applied in the diet analysis. and 0.71, with the exception of the location at 1,200 m, where it To measure the use of a resource (p ) compared with its availabil- was very low (0.39), and at 2,500 m, where it was very high (0.90). ity (q ), we calculated the Ivlev’s electivity index, E (Ivlev 1961): i i The frequency of each prey appearing in the diet did not signifi- p q i i E ¼ : cantly differ with elevation, except Formicidae (Table 3). p þ q i i Nonetheless, the consumption of Coleoptera increased with eleva- tion (q ¼ 0.94, P ¼ 0.005, n ¼ 6 locations). According to hardness, This index ranges from 1 to 1, with zero indicating random most of the prey consumed had a high degree of hardness (37.6%; selection, negative values indicating avoidance or inaccessibility of medium hardness: 31.2%; low hardness: 31.2%). Regarding eva- the prey item and positive values showing active selection. siveness, P. algirus consumed mainly prey with intermediate evasive- ness (43.3%), followed by prey with high evasiveness (32.5%), prey Statistical Analysis with low evasiveness being minor in the diet (24.2%). We discerned To compare the frequency of consumption of each OTU between no significant elevational pattern for consumption of prey according sexes or among elevations, or differences in availability between to their hardness or evasiveness (data not shown for simplicity). microhabitats, we used the Chi-squared test. For variables with a continuous distribution, such as number of prey per pellet or indi- Prey availability for P. algirus along the elevational vidual trophic niche width, we compared the 2 sexes and the various elevations (i.e., sampling points) with a 2-way factorial ANOVA, gradient considering the interaction elevation * sex. For comparisons A total of 14,793 individuals, from 19 different OTUs, were cap- between sexes restricted to the alpine zone, the t-test was used. To tured in 1,534 pitfalls-day (Table 4). All OTUs found in the lizard test for the average number of potential prey available per elevation, diet were recorded in pitfalls, except Pseudoscorpionida. By con- we performed an ANOVA, considering as the statistical unit each trast, 4 taxa recorded in pitfalls were not consumed by lizards: day the set of pitfall traps at a given elevation was activated at every Isopoda, Diplopoda, Collembola, and Zygentoma. Formicidae stand elevation (n ¼ 98). When we were interested in elevational patterns, out as the most abundant potential prey, 74% of the total, being Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Moreno-Rueda et al. Prey availability and selection in Psammodromus algirus 607 Table 1. Frequency (and percentage) of the different OTUs in the Table 4. Frequency (and percentage) of each OTU collected in the diet of P. algirus in the Sierra Nevada, as well as the number (and pitfall traps (n ¼ 1,534 traps-day), as well as number (and percent- percentage) of feces in which they were present age) of pitfalls in which each OTU was caught Frequency % Frequency Presence % Presence Frequency % Frequency Presence % Presence Orthoptera 90 19.78 57 79.17 Formicidae 10,970 74.16 1,062 71.04 Formicidae 87 19.12 13 18.06 Coleoptera 1,173 7.93 442 29.57 Coleoptera 58 12.75 33 45.83 Acarina 519 3.51 249 16.66 Hemiptera 52 11.43 30 41.67 Orthoptera 506 3.42 235 15.72 Araneae 42 9.23 39 54.17 Araneae 406 2.74 304 20.33 Larvae 28 6.15 17 23.61 Hemiptera 276 1.87 213 14.25 Hymenoptera 26 5.71 17 23.61 Hymenoptera 267 1.80 210 14.05 Embioptera 26 5.71 7 9.72 Diptera 162 1.10 109 7.29 Lepidoptera 18 3.96 18 25.00 Collembola 119 0.80 74 4.95 Other taxa 28 6.15 15 20.83 Diplopoda 100 0.68 36 2.41 Zygentoma 88 0.59 37 2.47 Notes: “Other taxa” includes OTUs that appeared <10 times: Acarina (9), Lepidoptera 65 0.44 45 3.01 Blattodea (7), Diptera (7), Pseudoscorpionida (2), Neuroptera larvae (2), and Isopoda 31 0.21 20 1.34 Mantodea (1). Larvae include those of unidentiﬁed taxa. Hymenoptera does Larvae 30 0.20 27 1.81 not include formicidae. N¼ 72 individual lizards. Embioptera 28 0.19 23 1.54 Blattodea 24 0.16 24 1.61 Neuroptera 17 0.11 17 1.14 Table 2. Frequency in males and females (n ¼ 36 in each cases) of Opilionida 9 0.06 9 0.60 the 5 most frequent OTUs in the diet of Psammodromus algirus Mantodea 3 0.02 3 0.20 Females Males v Notes: In the case of neuroptera, only larvae were captured. Hymenoptera ns Orthoptera 41 49 0.36 does not include formicidae. Larvae refer to those of unidentiﬁed taxa. ns Formicidae 49 38 0.70 ns Coleoptera 31 27 0.14 ns Table 5. Number of individuals of each OTU found in pitfall traps Hemiptera 24 28 0.15 ns under shrubs (n ¼ 768) and in open habitat (n ¼ 766) Araneae 25 17 0.77 Open Shrub v Note: Sexual differences in the frequency were checked with a Chi-squared ns test for each OTU; in no case were differences signiﬁcant ( P > 0.05). Formicidae 5,668 5,302 6.11* Coleoptera 686 487 17.01*** Araneae 229 177 3.34 Table 3. The frequency of the 5 most common OTUs in the diet of ns Orthoptera 262 244 0.32 P. algirus according to elevation (n ¼ 12 individual lizards at each Hemiptera 113 163 4.57* elevation) ns Hymenoptera 126 141 0.42 ns 300 700 1200 1700 2200 2500 v Lepidoptera 32 33 0.01 ns Larvae 16 14 0.07 ns Orthoptera 7 18 15 13 18 19 6.80 ns Embioptera 15 13 0.07 Formicidae 31 8 32 7 8 1 17.73** ns Coleoptera 4 10 5 11 13 15 9.60 Notes: The value of the Chi-squared testing for statistical differences between ns Hemiptera 10 9 6 6 13 8 4.00 ns microhabitats is shown; indicates non-signiﬁcant differences (P > 0.5); ns Araneae 7 5 7 4 9 10 3.71 P¼ 0.07; *P< 0.05; ***P< 0.001. Only OTUs that formed part of the diet of P. algirus were considered (see Table 1). Notes: Variation with elevation was tested with a Chi-squared test, whose ns values are shown in the table; indicates non-signiﬁcant (P > 0.05); lizards. Our analysis showed that the overall prey abundance signifi- **P < 0.01. cantly varied with elevation (F ¼ 6.92, P < 0.001; Figure 3), 5,92 showing a lineal increase (q ¼ 0.94, P ¼ 0.005). However, the rela- tive frequency of Araneae significantly decreased with elevation present in 71% of the pitfalls (Table 4). Excluding Formicidae, the most abundant potential prey for P. algirus were Coleoptera, (q¼0.89, P ¼ 0.019); the remaining OTUs showed no significant Orthoptera, Acarina, and Araneae (Table 4). These OTUs were, trend with elevation (Figure 4). together with Hemiptera and Hymenoptera, the most widely distrib- uted (collected in >10% of the pitfalls; Table 4). Hemiptera was Trophic niche width of P. algirus along the elevational more abundant under shrubs whereas Coleoptera and Formicidae gradient were more abundant in open areas (Table 5). For P. algirus in the Sierra Nevada, trophic niche width (standar- To analyze how prey abundance varies with elevation, we con- dized Levins’ index, Bs) was 0.497, suggesting an intermediate sidered only the OTUs most consumed by P. algirus (Orthoptera, amplitude. Trophic niche width increased with elevation (q ¼ 0.89, Coleoptera, Hemiptera, and Araneae). Formicidae was not consid- P ¼ 0.019; Figure 5), and with prey abundance in the locations ered, despite their high frequency in the P. algirus diet, because they (q ¼ 0.94, P ¼ 0.005). The diversity of available prey also increased were excessively abundant in pitfall traps, precluding analyses with elevation (q ¼ 0.83, P ¼ 0.042; Figure 5). Analyzing sexes sepa- (Greenslade 1973), and, moreover, given their small size and high degree of chitinization, they presumably provide low biomass to rately, we found that females showed greater diet width (i.e., they Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 608 Current Zoology, 2018, Vol. 64, No. 5 Figure 4. Relative abundance, according to elevation, of the main OTUs con- sumed by Psammodromus algirus (except Formicidae): Araneae (white), Orthoptera (hatched), Hemiptera (gray), and Coleoptera (black). Figure 3. Average number of overall items of the most consumed prey (Orthoptera, Hemiptera, Coleoptera, and Araneae), except Formicidae, col- lected daily in pitfalls according to elevation (masl). Bars indicate the 95% conﬁdence intervals. were more generalist) in the high- and lowlands, whereas males were more generalist in the midlands (Figure 5). In fact, the trophic niche width of the 2 sexes showed an inverse pattern across the loca- tions studied (q¼0.83, P ¼ 0.042; Figure 5). Considering the individual diet width (Bi), we found significant differences between sexes (F ¼ 5.97, P ¼ 0.017) and among eleva- 1,60 tions (F ¼ 2.51, P ¼ 0.039), which explained 15% of variation in 5,60 Bi (whole model: F ¼ 2.15, P ¼ 0.03, adjusted R ¼ 0.15). The 1,60 interaction was not significant (F ¼ 1.15, P ¼ 0.35). Females 5,60 showed a wider diet than did males (0.146 0.013 vs. 0.106 0.014; Figure 5. Trophic niche width (Bs) according to elevation (masl), as a whole mean6 SE), suggesting that females are more generalist. Regarding (squares and heavy black line), males (rhombus and dotted line) and females elevation, individual diet width was fairly stable up to 1,700 m, and (triangles and gray line). The diversity of available prey is indicated with then showed a lineal increase (Figure 6). Individual diet niche width crosses joined by a dotted line. correlated positively with elevation (q ¼ 0.83, P ¼ 0.042) and with total niche width (q ¼ 0.89, P ¼ 0.019). The average prey per pellet Diet of P. algirus in the alpine zone was 6.326 0.71 (mean6 SE) and did not vary with elevation In a more detailed analysis at the alpine zone (2,200 and 2,500 m), (F ¼ 0.77, P ¼ 0.58; data not shown for simplicity) or sex (males: 5,60 we recorded 14 OTUs in lizard feces (n ¼ 65 individuals), including 6.036 0.84; females: 6.596 1.15 prey per pellet; F ¼ 0.20, 1,60 2 OTUs not recorded in the sample previously analyzed for the com- P ¼ 0.66; sex * elevation: F ¼ 1.82, P ¼ 0.12). 5,60 plete elevational gradient: Diplopoda and Odonata (Table 6). The diet of alpine lizards was composed mainly of Orthoptera and Prey selection along the elevational gradient Coleoptera, which comprised almost 50% out of the prey (Table 6). We restricted the analysis of prey selection to the main prey of In comparison with the diet for the overall mountain, it was remark- P. algirus: Orthoptera, Coleoptera, Hemiptera, and Araneae. We able the low frequency of Formicidae in the alpine zone (only 6%), excluded Formicidae since, given their elevated abundance in pitfall the absence of Embioptera, and the higher importance of Blattodea traps, its inclusion in the analysis would provoke spurious results (almost 6%) (see Tables 1 and 6 to compare). There were no sex dif- (i.e., in comparison, the remaining prey will give positive election; ferences in number of prey per pellet (females: 7.336 0.71, males: Greenslade 1973). We did not consider less representative prey, 6.296 0.42; t ¼ 0.84, P ¼ 0.40, test carried out with data log- either. Our findings showed that electivity for Araneae increased transformed), or in the individual diet width (females: 0.196 0.018, with elevation (q ¼ 0.89, P ¼ 0.019), being negatively selected at males: 0.166 0.016; t ¼ 1.34, P ¼ 0.18). The Chi-squared test low elevations, and positively so at high elevations (Figure 7). revealed no differences in the diet between males and females (for Orthoptera was in all cases positively selected, except at 2,200 m, every OTUs, P > 0.10). which was the location with the highest abundance of Orthoptera (here we collected more Orthoptera than at all the other locations Discussion together). Indeed, selection for Orthoptera was negatively correlated with its absolute abundance in the locations (q¼0.89, P ¼ 0.019). The diet of P. algirus along the elevational gradient Hemiptera was also positively selected in every elevation, except at Psammodromus algirus consumed 17 different OTUs in the Sierra 1,200 m, where they were the dominant taxon (see Figure 4). Lastly, Nevada mountain (including Diplopoda and Odonata, reported in Coleoptera was negatively selected across the overall elevational the alpine subsample). The main components of the diet of this liz- gradient (Figure 7). ard were Orthoptera, Formicidae, Coleoptera, Hemiptera, and Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Moreno-Rueda et al. Prey availability and selection in Psammodromus algirus 609 Table 6. Frequency and percentage, separated by females (n ¼ 30) and males (n ¼ 35), of each OTU found in the feces of the lizard Psammodromus algirus in the alpine zone (2,200 and 2,500 masl) Females Males Frequency % Frequency Frequency % Frequency Orthoptera 44 20.09 63 28.64 Coleoptera 48 21.92 52 23.64 Hemiptera 22 10.05 24 10.91 Larvae 20 9.13 19 8.64 Araneae 19 8.68 19 8.64 Formicidae 20 9.13 8 3.64 Hymenoptera 16 7.31 10 4.55 Blattodea 13 5.94 13 5.91 Lepidoptera 8 3.65 9 4.09 Other taxa 9 4.11 3 1.36 Notes: Other taxa included 7 Acarina, 2 Diptera, 1 Diplopoda, 1 Odonata, Figure 6. Elevational variation in the individual trophic niche width (Bi) in the and 1 Mantodea. Hymenoptera does not include Formicidae. Larvae refer to lizard Psammodromus algirus. Bars indicate the 95% conﬁdence intervals. those of unidentiﬁed taxa. (Dı ´az and Carrascal 1993). Nonetheless, it probably is an attractive prey for this lizard given its size (Dı ´az and Carrascal 1990). It is pos- itively selected by this lizard, but its abundance is probably underes- timated in pitfall traps (Woodcock 2005), and therefore its electivity is probably lower than estimated. However, Orthoptera are not con- sumed simply according to its abundance in the environment; con- trarily, along the elevational gradient, its electivity is negatively correlated with total abundance. Hemiptera was other prey positively selected by this lizard at every elevation, except where it was the most abundant prey (at 1,200 m). Given that this is the most profitable prey for P. algirus (Dı ´az and Carrascal 1993), it remains intriguing why it is not more frequently consumed. Several Hemiptera are toxic (Blum 1981), and Figure 7. Values of the Ivlev’s electivity index for every elevation and for thus lizards perhaps limit their consumption (Vitt and Pianka 2007). every of the main OTUs consumed by P. algirus (except Formicidae): Araneae Coleoptera, despite being widely consumed (both in the Sierra (white), Orthoptera (hatched), Hemiptera (gray), and Coleoptera (black). Nevada and throughout the complete distribution range of P. algirus, Positive values indicate positive selection (i.e., prey were consumed more Table 7), was negatively selected considering its high availability. than expected by chance according to their availability in pitfalls) whereas Although with large size, they are very chitinous (Herrel et al. 2001), negative values indicate negative selection. Values of the index oscillate between 1 and þ1. and thus energy intake is constrained by the costs associated with han- dling time and digestion (Dı ´az and Carrascal 1993). Moreover, some Araneae, embracing 72.3% of prey types. These OTUs correspond of them are toxic, rich in alkaloids (Blum 1981), and lizards show to the main prey described in other studies throughout the distribu- aversion to alkaloids (Cooper et al. 2002), or even the scent of beetles (Cooper and Pe ´ rez-Mellado 2002). The consumption of Coleoptera tion range of the species (Table 7). The main prey were terrestrial arthropods, according to the foraging mode of P. algirus, actively increased with elevation, a pattern that was unrelated to their abun- searching for prey at the ground level. We detected subtle variation dance. Instead, it might be a consequence of the use of microhabitat in the diet along the elevational gradient, which is, however, small by lizards, which employ more time basking in open areas, the con- trary occurring at low elevations (Dı´az 1997;alsosee Zamora- in comparison with the wide variation in diet over the entire distri- bution range (see Table 7). For example, Diptera (minority prey in Camacho et al. 2016). Given that Coleoptera are more abundant in the Sierra Nevada) was an important part of the diet in several stud- open areas than under shrubs, this elevational change in microhabitat ies (Pe ´ rez-Quintero and Rubio-Garcı´a 1997; Rouag et al. 2007; use could boost the encounter rate with elevation. Alternatively, given Bouam et al. 2016), and Orthoptera proved to be the most impor- that P. algirus lizards are larger with elevation (Zamora-Camacho tant prey in the Sierra Nevada but was not relevant in several other et al. 2014a), they could easily consume hard prey. However, as a studies (Table 7). In general, the reason for these geographic differ- whole, the consumption of hard prey did not covary with elevation. Araneae are present with relevant frequency (>5%) in all studies ences is poorly known. Our study, in fact, compares 6 locations carried out along the distribution range of P. algirus (Table 7; with along a wide elevational gradient (2,200 m), allowing us to test some of the reasons for geographic variation in diet. the exception of Valverde ). Araneae are softly chitinous Orthoptera was the main prey of P. algirus along the elevational (Herrel et al. 2001) and may be very profitable for lizards (Dı ´az and gradient in the Sierra Nevada. It is an evasive prey, difficult to cap- Carrascal 1993), although some of them can be dangerous (and even ture, and probably to subdue and swallow (considering its hind may prey on lizards, Ho ´ dar and Sa ´ nchez-Pinero ~ 2002) and cursory limbs and wings), hence providing low profitability to P. algirus species may be difficult to capture. Its electivity increased with the Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 610 Current Zoology, 2018, Vol. 64, No. 5 Table 7. Literature review of the percentage of consumption of the most common prey (>5% frequency) in the diet of Psammodromus algirus according to different studies AB CD E F G H I J KL M N O P Q Coleoptera 13 52 38 17 14 31 5 16 28 17 25 34 7 14 24 26 Araneae 9 7 12 9 6* 7 20 8 7 13 10 18 16 12 14 10 Hemiptera 11 15 11 19 61 20 29 22 32 19 10 16 7 Formicidae 19 15 13 10 26 8 17 6 9 9 13 6 Orthoptera 20 7 9 13 19 6 17 6 13 Hymenoptera 6 10 6 6 6 6 9 12 9 17 Diptera 10 8 14 30 7 9 32 31 28 17 Larvae 6 13 13 38 11 8 Plecoptera 8 Phasmidae 7 Diplopoda 7 Embioptera 6 Collembola 5 Vegetal 23 Notes: A, this study; B, Valverde (1967);C, Mellado et al. (1975);D,Pe ´ rez-Mellado (1982); E, Di Palma (1984);F, Seva (1984); G, Pollo and Pe ´ rez-Mellado (1988); H, Dı´az and Carrascal (1990); I, Ortega-Rubio (1991);J, Gil (1992);K, Carretero (1993, Aiguesmolls); L, Carretero (1993, Torredembarra); M, Carretero and Llorente (1993);N,Pe ´ rez-Quintero and Rubio-Garcı´a(1997, El Rompido); O, Pe ´ rez-Quintero and Rubio-Garcı´a(1997, Asperillo); P, Rouag et al. (2007);Q, Bouam et al. (2016). Larvae include larvae of different taxa. Hymenoptera does not include formicidae. Vegetal refers to plant matter. *In this study the taxa reported is Arachnida. elevational gradient, following a reversed pattern with its relative achieved by preying on different prey types in order to cover a wide abundance. range of nutrients (Pe ´ rez-Mellado et al. 1991). This last explanation Formicidae, despite being the second most frequent prey, were would also explain why the diet of P. algirus was very similar along negatively selected when considering their enormous availability in the elevational gradient. the environment (>70% of available prey). Formicidae are small, Other possible patterns with elevation were not supported. First, highly chitinous, and potentially dangerous, and therefore P. algirus given that ability for prey capture improves with body temperature only occasionally consumed them, probably when the availability of (Dı ´az 1994a), and environmental temperature diminishes with ele- vation, so that the consumption of evasive prey would be expected other prey is very low. Like Formicidae, many other prey only occa- to decrease with elevation. This was not supported, but it should be sionally occurred in the diet of this lizard, small prey such as Acari (very abundant in the environment, but rarely consumed) or noted that lizard body temperature shows no change with elevation Collembola. This result is consistent with the idea that P. algirus in our study system (Zamora-Camacho et al. 2013, 2016). selects prey according to prey size rather than prey type (Dı ´az and Moreover, sprint speed of P. algirus does not vary with elevation in the Sierra Nevada (Zamora-Camacho et al., 2014b). In addition, liz- Carrascal 1990, 1993). Other prey, highly evasive (flying prey such ard body size increases with elevation in the Sierra Nevada as Hymenoptera, Lepidoptera, and Diptera) or chitinous (Diplopoda), also seemed not to be positively selected. However, (Zamora-Camacho et al. 2014a), and therefore, we predicted hard- Orthoptera and Coleoptera were the main prey of this lizard, and ness of prey to increase with elevation, but this prediction was not supported, either. they are highly evasive and hard, respectively. Therefore, other things should cause lizards not to consume flying prey and Diplopoda. Diplopoda is probably avoided as a consequence of its Trophic niche width repugnatorial glands more than as a consequence of its hardness. The parameter trophic niche width was intermediate, but increased Hymenoptera may be dangerous and is very chitinous, but with elevation. This pattern could be due to several reasons. First, Lepidoptera and Diptera probably would be adequate for P. algirus. P. algirus body size becomes greater with elevation (Zamora- However, if P. algirus forages mainly on the ground, its rate of Camacho et al. 2014a), and then the range of body sizes (see Dı ´az encounters with these flying prey is probably very low, while 1994b) and/or the number of prey consumed could increase with encounters with Orthoptera are much more frequent. Similarly, one elevation, augmenting niche width. Nevertheless, trophic niche of the most profitable prey for P. algirus are larvae (Dı ´az and width seems to decrease, rather than to increase, with body size in Carrascal 1993), but their abundance in the environment was low lizard species (Costa et al. 2008b). Moreover, the number of prey (Table 4), limiting their consumption. consumed per individual did not vary with elevation. Alternatively, As a whole, P. algirus feeds mainly on arthropods, behaving as a the diversity of competitors could decline with altitude, favoring a generalist species along its geographic range. Foraging behavior of niche release and greater trophic niche width (Comas et al. 2014). P. algirus, however, is not simply based on encounter rate. At least Effectively, the lizard community accompanying P. algirus for Hemiptera, Orthoptera, and Araneae, they are consumed in a (Psammodromus edwardsianus, Podarcis hispanicus, Timon neva- frequency contrary to their abundance. A pattern of negative corre- densis, Tarentola mauritanica, and Acanthodactylus erythrurus) lation between relative abundance and electivity is general in lizards shows a diminishing of diversity with elevation (Caro et al. 2010). and might be explained if lizards avoid toxic or dangerous prey Nevertheless, the clearest reason for the greater trophic niche width above a threshold (Carretero 2004). However, this pattern may also with elevation is a concomitant rise in prey diversity (Figure 5). be explained if lizards search for a balanced diet, which would be Moreover, the greater trophic niche width was the result of every Downloaded from https://academic.oup.com/cz/article-abstract/64/5/603/4741358 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Moreno-Rueda et al. Prey availability and selection in Psammodromus algirus 611 lizard increasing the diversity of prey consumed, as shown by a Funding correlation between both population and individual trophic niche This study was economically supported by the Ministerio de Ciencia e width. Therefore, our findings do not support the niche variation Innovacio ´ n (project CGL2009-13185). Two predoctoral grants (FPU pro- hypothesis. gram) from the Ministerio de Educacio ´ n (Ministry of Education) supported FJZC (ref: AP2009-3505) and SR (ref: AP2009-1325). IAB received a grant We found sex differences in trophic niche width, diet being more for initiation to the research by the University of Granada. varied in females than in males, which agrees with that found in a population from NE Spain (Carretero and Llorente 1993). This sex difference was not due to differences in the quantity of prey References consumed, which did not differ between sexes. The reason why Bearhop S, Adams C, 2004. Determining trophic niche width: a novel females are more generalist remains unknown and is remarkable, approach using stable isotope analysis. J Anim Ecol 73:1007–1012. given that, as was explained in the “Introduction,” we expected a Belliure J, Carrascal LM, Dı´az JA, 1996. Covariation of thermal biology and wider trophic niche in males. One possibility is that females need a foraging mode in two Mediterranean lacertid lizards. Ecology 77: higher diversity of resources for reproduction, especially egg forma- 1163–1173. tion. For example, Navarro-Lo ´ pez et al. (2014) reported that diet Blum MS, 1981. Chemical Defenses of Arthropods. New York: Academic Press. width improves reproductive success in the common kestrel (Falco Bolnick DI, Svanback R, Arau ´ jo MS, Persson L, 2007. Comparative support tinnuculus). We also found an inverse interpopulation relationship for the niche variation hypothesis that more generalized populations also between male and female niche width (Figure 5), which could sug- are more heterogeneous. Proc Nat Acad Sci USA 104:10075–10079. gest certain niche segregation, but we failed to find sex differences in Bouam I, Necer A, Saoudi M, Tahar-Chaouch L, Khelfaoui F, 2016. Diet and diet (Table 2). Other studies found a similar absence of sex differen- daily activity patterns of the lacertid lizard Psammodromus algirus (Sauria: ces in diet in this species (Pollo and Pe ´ rez-Mellado 1988; Pe ´ rez- Lacertidae) in a semi-arid Mediterranean region. Zool Ecol 26:244–252. Quintero and Rubio-Garcı´a 1997). Indeed, diet overlap was rela- Brunner FS, Schmid-Hempel P, Barribeau SM, 2014. Protein-poor diet reduces tively high. host-speciﬁc immune gene expression in Bombus terrestris. Proc R Soc B 281:20140128. Caro J, Ferna ´ ndez Cardenete JR, Benı ´tez M, Chirosa M, Zamora-Camacho FJ Adaptation to the alpine environment et al., 2010. Estudio de Anﬁbios y Reptiles en el Espacio Natural de Sierra The alpine environment is harsh for ectotherms. Moreover, it marks Nevada, en el Marco del Cambio Global. Unpublished Report. Universidad the elevational limit for P. algirus, and therefore, it is expected to be de Granada. Carretero MA, 1993. Ecologı´a de los lace ´ rtidos en arenales costeros del nor- a marginal habitat for which the lizard is poorly adapted. However, este ibe ´ rico [PhD thesis]. Universitat de Barcelona. the results indicate that the alpine habitat is not suboptimal for Carretero MA, 2004. From set menu to a la carte. Linking issues in trophic P. algirus, as diet in alpine environments for this species proves very ecology of Mediterranean lacertids. Ital J Zool 71:S121–S133. similar to that at lower elevations, and, in fact, prey abundance and Carretero MA, Llorente GA, 1993. Feeding of two sympatric lacertids in a diversity are the highest in the alpine zone. Time available for forag- sandy coastal area Ebro Delta (Spain). In: Valakos ED, editor. Lacertids of ing decreases with elevation (Zamora-Camacho et al. 2013). the Mediterranean Region. A Biological Approach. Atenas: Hellenic However, at highlands, there is a burst of resources that lizards seem Zoological Society, 155–172. to exploit to reach high densities, almost as high as at midlands, and Comas M, Escoriza D, Moreno-Rueda G, 2014. Stable isotope analysis reveals variation in trophic niche depending on altitude in an endemic alpine gecko. much higher than in the lowlands (see Zamora-Camacho et al. Basic Appl Ecol 15:362–369. 2013). 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“My last article couldn't be possible without the platform @deepdyve that makes journal papers cheaper.”@JoseServera