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Breadth and overlap of diet between syntopic populations of parthenogenetic Aspidoscelis tesselata C and gonochoristic Aspidoscelis sexlineata (Squamata: Teiidae) in southeastern Colorado.

East of the Rocky Mountains in Colorado, gonochoristic (Tomlinson, 1968) Aspidoscelis sexlineata is distributed widely, whereas parthenogenetic A. tesselata (pattern class C) has been recorded from relatively small areas of only three southeastern counties (Walker et al., 1997; Hammerson, 1999). Distributions of these lizards in Colorado reflect different tolerances for climatic, edaphic, topographic, and vegetational variables (walker et al., l998), largely stemming from different modes of evolutionary origin. Derivation of the allodiploid genome of A. tesselata in either northern Mexico or southern Texas from A. tigris marmorata X A. gularis septemvittata (Neaves, 1969; Parker and Selander, 1976; Dessauer and Cole, 1989) did not hamper its dispersal northward to otero and Las Animas counties, Colorado (Parker and Selander, 1976). However, lack of further expansion northward, based largely on this allodiploid genome, coincides with northwestward dispersal of Aspidoscelis neotesselata, a triploid parthenogenetic species of recent origin from A. tesselata X A. sexlineata (Parker and Selander, 1976; Densmore et al., 1989), beyond the range of A. tesselata into pueblo and Fremont counties (walker et al., 1997; Taylor et al., 2006).

Coexistence of A. tesselata C and A. sexlineata in southeastern Colorado provided an opportunity to compare diets between congeners with strikingly different reproductive modes, size of adults, and evolutionary histories. our study addressed the following questions: Do syntopic populations of A. tesselata C and A. sexlineata have similar breadths of diet? Does breadth of diet change across months and years? Are there significant differences between observed dietary overlaps and overlaps predicted by chance? Are breadths of diets of A. tesselata C and A. sexlineata in Colorado similar to those reported for A. tesselata E and different gonochoristic congeners in Trans-Pecos, Texas (Schall, 1993)?

Materials and Methods--Specimens were pooled from three localities in Ninemile Valley, Otero County, Colorado (described by Walker and Cordes, 1998); HVC was 4.3 km SW Colorado Highway 109 on road 804; H-SR was 8.6-9.0 km SW Colorado Highway 109 on road 804; and H-NV was 11.5-13.4 km SW Colorado Highway 109 on road 804 (approximate center of this site was at UTM 13S 630854E, 4175545N, WGS84 datum). Specimens listed by date are: 9-10 July 1988, Aspidoscelis tesselata C, university of Arkansas Department of Zoology (UADZ) 3147, 3155, 3156, 3159, 3160, 3182, 3184, 3185, 3187, 3188, 3194-3196, 3198, 3199, 3203 (n = 16, 3195 and 3198 had empty stomachs) and A. sexlineata viridis, UADZ 3148, 3152-3154, 3157, 3158, 3163-3165, 3179-3181, 3190, 3191, 3197, 3200 (n = 16); 11 August 1988, A. tesselata C, UADZ 3409-3412, 34143423 (n = 14); 4-5 June 1990, A. tesselataC, UADZ 4088, 4090-4093, 4104-4106, 4108, 4109, 4111-4113, 4115-4117 (n = 16) and A. sexlineata viridis, UADZ 4077-4087, 4089, 4124-4127, 4130 (n = 17, 4084 had an empty stomach). There was no apparent ecological difference between localities. Habitat was characterized by scattered shrubs including Chrysothamnus nauseosus (rabbitbrush), Sarcobatus vermiculatus (greasewood), and Gutierrezia sarothrae (snakeweed), and an assortment of weeds on the roadside and severely deteriorated grassland of the Ninemile Valley adjacent to road 804 (Walker et al., 1998: figure 3). In addition to A. tesselata C and A. sexlineata, other Aspidoscelis at this locality included A. tesselata D and A. neotesselata B. small samples precluded inclusion of A. tesselata D and A. neotesselata B in our study. The historical significance of this four-member guild in resolving diverse problems involving parthenogenetic Aspidoscelis is summarized by Walker and Cordes (1998).

Adults of A. tesselata C and A. sexlineata were collected as encountered in July 1988 and June 1990. Stomach contents were removed, labeled, and stored in 70% ethanol. stomach contents were separated into taxonomic orders and counts and volumetric measurements were made to estimate breadth and overlap of diets. in small graduated cylinders, volumetric measurements of each category of prey were made by displacement in liquid.

We compared overlap in diet between A. tesselata C and A. sexlineata for each sampling period with expected values for overlap due to chance. Expected values were derived from a null model recommended by Winemiller and Pianka (1990) and available as alternative RA3 (Randomization Algorithm 3) in the Niche Overlap module of Ecosim700 software (http:// homepages.together.net/~gentsmin/ecosim.htm). Because breadth of diet for each species was retained in this model, results of simulation were not biased by small samples (Gotelli and Entsinger, 2001). We estimated overlap of diets using the symmetrical formula of Pianka (1973) and running 1,000 iterations of the simulation to obtain a mean value. Food items were assumed to be equally usable by both species by random, multiple, reshuffles of each row of the resource matrix. We used Levin's measure of breadth of niche: B = 1/[summation][p.sub.ij.sup.2], where [p.sub.ij] was the proportion of a particular taxon (i) in the diet of species j (Levins, 1968). Breadth of niche ranges from 1 to n, and B would be maximized at n with equivalent use of all taxa in the sample.

Because adults of A. tesselata C were much larger than adults of A. sexlineata (snout-vent length in mm: June 1990, 87.6 [+ or -] 4.1 SE and 69.3 [+ or -] 1.1 SE; July 1988, 88.1 [+ or -] 3.6 SE and 67.2 [+ or -] 1.6 SE, respectively), there was a possibility that food resources were being partitioned by size of prey. We tested this possibility by dividing total volume (cc) of each category of prey by number of individual prey in that category for each of the two species of lizards in each sample (June and July). This provided average size (cc) of individual prey in each category for informal interspecific comparisons. We also calculated the grand mean volume of prey in each month for each species and used t-tests to determine if there were significant interspecific differences in overall size of foods that were consumed.

Results--Assuming that samples obtained in July 1988 and June 1990 were representative of availability of prey for these months, both species increased use of grasshoppers in July (Tables 1 and 2). For A. tesselata C, the shift was from 3.1% in June to 45.8% in July (number of grasshoppers) or 11.3% in June to 81% in July (volume of grasshoppers). The shift to grasshoppers by A. sexlineata was from 16.8% in June to 37.3% in July (number of grasshoppers) or 52.3% in June to 77.3% in July (volume of grasshoppers). Adult beetles also were important to both species in July, as suggested by both number and volume (Tables 1 and 2). As in June, number of prey for July provided a broader estimate of diet for A. sexlineata (4.68) compared to A. tesselata C (3.82), but volume reduced the magnitude of the interspecific difference (1.62 for A. sexlineata and 1.50 for A. tesselata C). In contrast to samples in June, overlap in diets calculated from numbers (0.95) and volumes (1.00) were too high to be explained by chance (Table 3; P < 0.01). The general pattern was broader diet and less overlap in June and diets that were less diverse with greater overlap in July.

Numbers of individual prey (Table 1) indicated that principal foods of A. tesselata C were caterpillars (Lepidoptera 35.2%), adult beetles (Coleoptera 13.3%), and bugs (Hemiptera 10.2%), and principal foods of A. sexlineata were spiders (Araneae 16.8%), grasshoppers (orthoptera 16.8%), and leaf hoppers (Homoptera 14.1%). Volumes of prey consumed (Table 2) were broadly congruent with numbers of individual prey in identifying caterpillars as the principal food of A. tesselata C (48.1%) and grasshoppers as the principal food of A. sexlineata (52.3%). Numbers of prey items and volumes of prey categories both showed that three of the top four taxa of prey of A. tesselata C were caterpillars, adult beetles, and leaf hoppers, and that three of the top four taxa of prey of A. sexlineata were grasshoppers, leaf hoppers, and spiders (Tables 1 and 2). However, numbers and volumes provided contradictory information on breadth of dietary niches. Based on number of individual prey, A. sexlineata had a broader diet (9.24) than A. tesselata (5.81), but breadth of diets calculated from volumetric data did not appear to be significantly different between A. sexlineata (3.0) and A. tesselata C (3.54). overlaps in diets calculated from numbers of individual prey (0.56; P = 0.15) and volumes (0.38; P = 0.08) could be explained by chance (Table 3), i.e., as would be expected in the absence of interspecific interactions such as competition.

Aspidoscelis tesselata C and A. sexlineata had not partitioned food resources by size as evidenced by similar mean sizes of prey in each food category (Table 4). We tested this hypothesis by using mean size of prey as a variable and by comparing the grand means. Although A. tesselata C had a much larger body than A. sexlineata, overall mean size of prey was larger for A. sexlineata, both in June (A. tesselata C: 0.81 [+ or -] 0.28 cc; A. sexlineata: 0.95 [+ or -] 1.30 cc) and in July (A. tesselata C: 1.04 [+ or -] 1.23 cc; A. sexlineata: 1.40 [+ or -] 1.59 cc). However, this difference in mean size of prey was not significant (June, [t.sub.18] = 0.781, P = 0.78; July, [t.sub.12] = 0.642; P = 0.64).

Discussion--Diets in gonochoristic A. sexlineata and parthenogenetic A. tesselata have been studied (Paulissen, 1987; Paulissen et al., 1993, 1997, 2006), but this is the first comparison for syntopic populations of these species. schall (1993) determined from volumes of prey that A. tesselata E had a narrower breadth of diet than three sympatric, gonochoristic congeners in Trans-Pecos Texas. Although we reached a different conclusion based on volumes of prey consumed by A. tesselata C and A. sexlineata, the two studies cannot be compared directly. unlike our study, shall (1993) increased samples by pooling individuals of each species: A. tesselata E (n = 50), A. tigris marmorata (n = 66), A. gularis gularis (n = 81), and A. inornata heptagramma (n = 120) that had been collected during 4 months in each of 2 years from 45 sites (breadth of diet) and 5 sites (overlap of diet). This provided a broad, general perspective of diets for species in Trans-Pecos Texas. Shall (1993) also detected that A. inornata, a small species similar in size to A. sexlineata, was using smaller prey than A. tesselata E. in contrast, we revealed that A. sexlineata and A. tesselata C were using prey of similar size.

one point of similarity between assemblages of Aspidoscelis from Trans-Pecos Texas and Ninemile Valley was the high overlap in diets between A. tesselata C and gonochoristic congeners. However, high overlaps in diet in Trans-Pecos Texas were based on abundance of termites throughout the activity season (schall, 1993); high overlap of diets in Ninemile Valley was based on seasonal abundance of grasshoppers. The reliable presence of large numbers of termites that served as principal prey for Aspidoscelis in Trans-Pecos Texas (and for A. tesselata C and E at Sumner Lake, DeBaca County, New Mexico; Paulissen et al., 2006) was missing at our study site. Extensive overlap in diets did not imply competition among congeners in either study because these broadly overlapping diets resulted from opportunistic targeting of a particularly abundant prey.

Evidence suggests that A. tesselata might be at an ecological disadvantage compared to gonochoristic congeners. For example, A. tesselata E was less responsive than gonochoristic A. tigris marmorata to simulated predatory threats in the field (Price, 1992), and density of A. tesselata E did not increase in response to a systematic removal of A. tigris marmorata, a potential competitor, from a site of syntopy in southern New Mexico (Price et al., 1993). In addition, individuals of A. tesselata E had a higher parasitic load than those of A. tigris marmorata in samples collected from syntopic populations (Mata-Silva et al., 2008). This difference, along with similar findings for parthenogenetic and gonochoristic Heteronotia (Moritz et al., 1991), is related to the Red Queen hypothesis (Van Valen, 1973), i.e., the continuous generation of genetic variation in gonochoristic species has adaptive value in countering parasitic infection. Tangential evidence of ecological vulnerability in a parthenogen is provided by the isolated group of A. dixoni C in southwestern New Mexico (a parthenogenetic species derived from A. tesselata subsequent to the hybridization origin of A. tesselata; Cordes and Walker, 2006). Aspidoscelis dixoni C is possibly in a late stage of contraction of range, extirpation, or both, from effects of a recent expansion of gonochoristic A. tigris punctilinealis into its range (Cole et al., 2007). Despite negative connotations of this evidence, A. tesselata has a geographic distribution spanning ca. 1,100 km between our study site in otero County, Colorado (UTM 13S 630919E, 4175489N; WGS 84), and the southern limit of its range near saucillo (UTM 13R 467649E, 3100708N; WGS 84), Chihuahua, Mexico (Taylor et al., 2003). Within its range, A. tesselata coexists with an assortment of congeners, including parthenogenetic A. exsanguis, A. dixoni, A. neomexicana, A. neotesselata B, A. uniparens, and A. velox, and gonochoristic A. gularis gularis, A. g. septemvittata, A. inornata, A. sexlineata, and A. tigris marmorata. its extensive latitudinal range and successful assimilation into an array of taxonomically diverse communities are indicators of ecological success.

Based on nearly equal numbers of A. tesselata C and A. sexlineata in our samples (individuals were collected as they were encountered), it was not obvious that fitness of A. tesselata C had been affected negatively at Ninemile Valley. We detected no evidence of competition between the two species in either sampling period. For samples collected in June, overlap in diet could be explained by chance, and the extensive overlap in diet in July reflected an opportunistic response of both species to an increase in availability of grasshoppers.

Samples were collected under authority of Colorado Division of Wildlife Scientific Collection License 890256 issued to JEC. Financial support was provided by the Department of Biological Sciences and Fulbright College of Arts and Sciences, University of Arkansas. We thank J. A. Lemos-Espinal for providing the Spanish resumen.

Submitted 15 September 2009. Accepted 15 October 2010. Associate Editor was Geoffrey C. Carpenter.

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HARRY L. TAYLOR, * MARK A. PAULISSEN, JAMES M. WALKER, AND JAMES E. CORDES

Department of Biology, Regis University, Denver, CO 80221 (HLT) Department of Natural Sciences, Northeastern State University, Tahlequah, OK 74464 (MAP) Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701 (JMW) Division of Sciences and Mathematics, Louisiana State University, Eunice, LA 70535 (JEC)

* Correspondent: htaylor@regis.edu
TABLE 1--Percentages of the total number of food items in stomachs
of adult parthenogenetic Aspidoscelis tesselata C and gonochoristic
A. sexlineata from a site of syntopy in Ninemile Valley, Otero County,
Colorado.

                            June 1990

                  A. tesselata    A. sexlineata
Food item            n = 16           n = 16

Araneae                5.5            16.8
Scorpiones             0.0             0.9
Solifugae              0.8             0.0
Opiliones              0.0             1.8
Isopoda                2.3             0.0
Microcoryphia          0.0             0.0
Collembola             0.0             0.0
Orthoptera             3.1            16.8
Isoptera               3.9             1.8
Hemiptera             10.2             5.3
Homoptera              7.8            14.1
Coleoptera
  Adults              13.3             4.4
  Larvae               5.5            11.5
Lepidoptera
  Adults               4.7             2.7
  Larvae              35.2             8.0
Diptera                0.8             1.8
Hymenoptera            0.8             2.7
Insect pupae           4.7             4.4
Snails                 0.0             5.3
Unidentified           1.6             1.8

Number of prey       128.0           113.0

                             July 1988

                  A. tesselata    A. sexlineata
Food item            n = 14           n = 16

Araneae                6.8             9.8
Scorpiones             0.0             0.0
Solifugae              0.0             0.0
Opiliones             10.2             2.0
Isopoda                6.8             9.8
Microcoryphia          0.0             2.0
Collembola             1.7             0.0
Orthoptera            45.8            37.3
Isoptera               0.0             0.0
Hemiptera              0.0             2.0
Homoptera              3.4             2.0
Coleoptera
  Adults              17.0            21.5
  Larvae               1.7             0.0
Lepidoptera
  Adults               0.0             2.0
  Larvae               3.4             2.0
Diptera                1.7             2.0
Hymenoptera            1.7             7.8
Insect pupae           0.0             0.0
Snails                 0.0             0.0
Unidentified           0.0             0.0

Number of prey        59.0            51.0

TABLE 2--Volumetric percentages of food items in stomachs of adult
parthenogenetic Aspidoscelis tesselata C and gonochoristic A.
sexlineata from a site of syntopy in Ninemile Valley, Otero County,
Colorado.

                                June 1990

                       A. tesselata    A. sexlineata
    Food item             n = 16           n = 16

Araneae                     1.8             5.3
Scorpiones                  0.0             0.1
Solifugae                   0.6             0.0
Opiliones                   0.0             0.1
Isopoda                     0.8             0.0
Microcoryphia               0.0             0.0
Collembola                  0.0             0.0
Orthoptera                 11.3            52.3
Isoptera                   <0.1            <0.1
Hemiptera                   1.1             0.1
Homoptera                  15.1            20.5
Coleoptera
  Adults                    9.2             1.7
  Larvae                    0.9             1.7
Lepidoptera
  Adults                    7.5            11.4
  Larvae                   48.1             3.2
Diptera                     0.8             0.8
Hymenoptera                <0.1            <0.1
Insect pupae                2.5             2.5
Snails                      0.0             0.4
Unidentified                0.2             0.1

Volume of prey (cc)        23.9            23.7

                                 July 1988

                       A. tesselata    A. sexlineata
    Food item             n = 14           n = 16

Araneae                     0.2             2.4
Scorpiones                  0.0             0.0
Solifugae                   0.0             0.0
Opiliones                   2.1             0.4
Isopoda                     1.3             2.0
Microcoryphia               0.0             0.1
Collembola                 <0.1             0.0
Orthoptera                 81.0            77.3
Isoptera                    0.0             0.0
Hemiptera                   0.0             0.1
Homoptera                   0.2             0.1
Coleoptera
  Adults                    8.9            12.3
  Larvae                    0.1             0.0
Lepidoptera
  Adults                    0.0             1.8
  Larvae                    5.2             3.2
Diptera                     0.9             0.1
Hymenoptera                 0.1             0.1
Insect pupae                0.0             0.0
Snails                      0.0             0.0
Unidentified                0.0             0.0

Volume of prey (cc)        21.4            17.1

TABLE 3--Comparison of dietary breadth (Levins, 1968) and overlap
(Pianka, 1973) between samples of adult parthenogenetic
Aspidoscelis tesselata C and gonochoristic A. sexlineata from a
site of syntopy in Ninemile Valley, Otero County, Colorado.

                                              June 1990

         Food parameter          A. tesselata          A. sexlineata

Numbers of prey
  Breadth of diet                    5.33                  9.24
  Overlap observed                              0.56
  Overlap expected from chance                  0.42
  Probability that observed
    overlap was explained
    by chance                                   0.15

Volumes of prey
  Breadth of diet                    3.54                  3.00
  Overlap observed                              0.38
  Overlap expected from chance                  0.18
  Probability that observed
    overlap was explained
    by chance                                   0.08

                                              July 1988

         Food parameter          A. tesselata            A. sexlineata

Numbers of prey
  Breadth of diet                    3.82                    4.68
  Overlap observed                               0.95
  Overlap expected from chance                   0.32
  Probability that observed
    overlap was explained
    by chance                                   <0.01

Volumes of prey
  Breadth of diet                    1.50                    1.62
  Overlap observed                               1.00
  Overlap expected from chance                   0.10
  Probability that observed
    overlap was explained
    by chance                                   <0.01

TABLE 4--Average size of prey (in cc) consumed by adult
parthenogenetic Aspidoscelis tesselata C and gonochoristic A.
sexlineata from a site of syntopy in Ninemile Valley, Otero County,
Colorado. Numbers in parentheses are sample sizes.

                          June 1990

Food item       A. tesselata    A. sexlineata

Araneae           0.26 (7)         0.28 (19)
opiliones
isopoda
orthoptera        2.82 (4)         2.75 (19)
isoptera          0.01 (5)         0.01 (2)
Hemiptera         0.08 (13)        0.01 (6)
Homoptera         1.50 (10)        1.30 (16)
Coleoptera
  Adults          0.54 (17)        0.34 (5)
  Larvae          0.13 (7)         0.13 (13)
Lepidoptera
  Adults          1.25 (6)         3.80 (3)
  Larvae          1.07 (45)        0.35 (9)
Insect pupae      0.42 (6)         0.51 (5)

                          July 1988

Food item       A. tesselata    A. sexlineata

Araneae           0.05 (4)         0.48 (5)
opiliones         0.35 (6)         0.40 (1)
isopoda           0.32 (4)         0.40 (5)
orthoptera        3.00 (27)        4.10 (19)
isoptera
Hemiptera
Homoptera         0.10 (2)         0.12 (1)
Coleoptera
  Adults          0.89 (10)        1.12 (11)
  Larvae
Lepidoptera
  Adults
  Larvae          2.58 (2)         3.20 (1)
Insect pupae
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Author:Taylor, Harry L.; Paulissen, Mark A.; Walker, James M.; Cordes, James E.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1U8CO
Date:Jun 1, 2011
Words:4156
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