Effects of habitat fragmentation on population structure of dune-dwelling 1, 2 1 DANIELLE K. WALKUP, DANIEL J. LEAVITT, AND LEE A. FITZGERALD

1Biodiversity Research and Teaching Collections, Department of Wildlife and Fisheries Sciences, A&M University, College Station, Texas 77843 USA 2Arizona Game and Fish Department, 5000 West Carefree Highway, Phoenix, 85086 USA

Citation: Walkup, D. K., D. J. Leavitt, and L. A. Fitzgerald. 2017. Effects of habitat fragmentation on population structure of dune-dwelling lizards. Ecosphere 8(3):e01729. 10.1002/ecs2.1729

Abstract. Landscape fragmentation alters biotic and abiotic characteristics of landscapes, variously affecting the size and demographic structure of ’ populations. Fragmentation is predicted to negatively impact habitat specialists because of perturbations to their habitat, whereas generalists should be less sensitive to fragmentation. Differences in life history among the lizards in this community should partly explain some of the variation in generalist species’ responses to fragmentation. During five seasons (2009–2013), we captured eight species of lizards on 27 independent trapping grids located in unfrag- mented (N = 18) and fragmented (N = 9) grids in the Mescalero-Monahans Sandhills ecosystem in south- eastern New . Using a two-way ANOVA, we tested for effects of fragmentation and year on capture rates for each species. To test for effects of fragmentation on demographic structure, we used contingency tables with expected frequencies computed from the demographic structure on unfragmented grids. Cap- ture rates of the endemic habitat specialist Sceloporus arenicolus (dunes sagebrush ) decreased to zero in fragmented sites. The demographic structure of S. arenicolus and maculata (common lesser ear- less lizard) was severely disrupted at fragmented sites, with proportions of juveniles, adult males, or adult females being over- or underrepresented during sample months. Variable responses of five generalist spe- cies could be attributed to life history patterns, habitat affinity, and breeding phenology. This is the first empirical study we are aware of that describes and quantifies the demographic effects of fragmentation on populations of multiple lizard species in a replicated study. Our findings lend important insights into how habitat specialization and differences in life history influence the susceptibility of species to the impacts of fragmentation.

Key words: Aspidoscelis; demography; ecological specialist and generalist; Holbrookia maculata; oil and gas development; Sceloporus arenicolus; Uta stansburiana.

Received 17 December 2016; accepted 18 January 2017. Corresponding Editor: Scott Carleton. Copyright: © 2017 Walkup et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected]

INTRODUCTION (Haila 2002, Fahrig 2003). Fragmentation can cause population declines in vulnerable species by Habitat loss and landscape fragmentation are disrupting processes such as dispersal, gene flow, considered primary drivers of biodiversity loss recruitment, and survival (Hokit and Branch 2003, (Brooks et al. 2002, Dirzo and Raven 2003, Bellard Henle et al. 2004, Mitrovich et al. 2009). However, et al. 2014). However, studies of vertebrate and broad variations in species’ specific responses to invertebrate communities show that individual fragmentation have made it difficult to identify species respond to landscape fragmentation differ- general trends that predict how a species may ently; some species thrive, while others decline respond to fragmentation (Betts et al. 2014).

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In an attempt to identify general trends in spe- very low proportions of juveniles the next spring cies’ responses to fragmentation, Andren et al. (Alcala and Brown 1967, Tinkle 1973, Dunham (1997) and Henle et al. (2004) predicted that habi- and Miles 1985, Barbault and Mou 1988). Alter- tat specialists would be more sensitive to frag- natively, some species maintain higher propor- mentation because they are dependent upon tions of juveniles throughout the year which may relatively restricted habitat types. Alternatively, be attributed to a still relatively high fecundity, habitat generalists are likely to be less sensitive to slower maturation, and longer life spans (Turner fragmentation and may even thrive in disturbed et al. 1969). Species with longer life spans, later and changing landscapes because of their broader age at maturity, and lower fecundity are charac- habitat tolerances, benefitting from the increased terized by population structures with almost landscape heterogeneity, more edge habitat, and equal proportions of adults and juveniles (Ballin- competitive relaxation associated with fragmenta- ger 1973, Stearns 1992). We propose that small tion (Henle et al. 2004, Devictor et al. 2008). This populations are susceptible to disruptions of age prediction has been supported in taxonomic or stage structure of both sexes (hereafter, demo- groups, such as birds and insects (Warren et al. graphic structure) as a result of landscape frag- 2001, Kotze and O’Hara 2003, Goulson et al. 2005, mentation. However, because of the interplay Devictor et al. 2008), and has been identified as a between life history, breeding phenology, and good predictor for some species (Mac habitat affinity among species, effects of frag- Nally and Brown 2001, Hibbitts et al. 2009). mentation should manifest differently for the However, this dichotomy does not describe all the different species in an ecological community. variation seen in the responses of lizards to frag- The consequences of landscape fragmentation mentation, and generalist species can also show may be exacerbated in ecosystems that are declines in fragmented areas (e.g., Driscoll 2004, naturally patchy and may affect the population Attum et al. 2006). As such, the contrast between dynamics or persistence of species adapted to liv- habitat specialists and generalists could be a use- ing in patchy habitats (Ryberg et al. 2013, 2015). ful framework, if integrated with other character- The Mescalero-Monahans Sandhills ecosystem, istics of the species, in predicting the likelihood of located in southeastern and adja- lizard species being sensitive to fragmentation. cent west Texas, overlying the Permian Basin, is Theory predicts that a typical population is comprised of ancient parabolic dunes maintained characterized by a relatively stable age structure by wind, moving sand, and partially stabilized and sex ratio, with natural seasonal fluctuation by Quercus havardii (shinnery oak; Hall and (Fitzgerald 1994, Gotelli 1995, Caswell 2001, Le Goble 2008). The system is characterized by a Galliard et al. 2005). In species that experience patchy arrangement of open dune blowouts seasonal birth pulses, including many lizard (bowl-shaped depressions formed when sand is species in temperate areas, the age structure cor- blown against the leeward slope with vegetated responds to a predictable yearly phenology, with arms extending around the sides) in a matrix of relatively high proportions of adults and young- shinnery oak flats (Fitzgerald and Painter 2009, of-year at the beginning of the breeding season, a Ryberg et al. 2015). Networks of roads built for peak in the proportion of adults during the mid- oil and gas development result in persistent land- dle of the breeding season as juveniles mature, scape fragmentation (Smolensky and Fitzgerald and a peak in proportions of juveniles near the 2011, Leavitt and Fitzgerald 2013; Fig. 1), and end of the breeding season as hatchlings emerge these fragmented areas have more compact soils, (Bustard 1969, Fitzgerald et al. 1999). Over many shallower slopes, and less shinnery oak, which years, the age structure is expected to be stable, are strong indicators of degraded dune blowout despite the seasonal changes. landforms in this habitat (Hibbitts et al. 2013). However, age or stage structure varies among The lizard community in this system is com- species and is strongly associated with their life posed of species ranging from widespread history strategies. Populations of species with generalists to an endemic habitat specialist early maturation, short life span, and high fecun- (Table 1). To date, much work has focused on dity have relatively high proportions of juveniles Sceloporus arenicolus (dunes sagebrush lizard), an after reproduction has occurred, which reverts to endemic habitat specialist threatened by loss and

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Fig. 1. Map of the study area identifying the location of 27 trapping grids in southeastern New Mexico. The aer- ial images show trapping sites. Sites were classified as fragmented when the density of oil well pads was >13.0 well pads/section (259 ha). (a) An unfragmented site with one well pad and (b) a fragmented site with 61 well pads. degradation of shinnery oak dunes. This habitat shown population dynamics of S. arenicolus are specialist requires dune blowouts, which are an particularly sensitive to configuration and condi- emergent landform maintained by complex inter- tion of the dune blowout landforms (Smolensky actions among wind, sand, and the shinnery oak and Fitzgerald 2011, Ryberg et al. 2013, 2015), (Ryberg et al. 2015). While previous work has they are not the only species in this lizard

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Table 1. Total captures and capture rates (mean captures/trap-day/grid) of eight species of lizard sampled on 27 trapping grids in unfragmented and fragmented sites during 2009–2013.

Total captures Capture rates Æ SD SVL at Max Clutch size† Clutches Max Family maturity SVL (eggs per per age Habitat Unfragmented Fragmented Species (mm) (mm) clutch) season (yr) affinity† (n = 18) (n = 9)

Phrynosomatidae Holbrookia maculata 44† 75† 2.98–6.1 1–2‡ 5† Generalist: 231 34 Grasslands 0.0045 Æ 0.0042 0.0012 Æ 0.0019 Sand dunes Phrynosoma cornutum 68† 86 23–30 >1† 10† Generalist§: 34 23 Deserts 0.0006 Æ 0.0005 0.0008 Æ 0.0009 Grasslands Sand dunes Sceloporus arenicolus 43 63 5.1 1–2‡ 4‡ Specialist: 1390 31 Sand dunes 0.0148 Æ 0.0198 0.0011 Æ 0.0014 Sceloporus consobrinus 44 62 7.2–9.9 1–3‡ 4† Generalist: 173 59 Woodlands 0.0027 Æ 0.0022 0.0020 Æ 0.0016 Deserts Grasslands Uta stansburiana 39 59 2–52–3† 3† Generalist: 11,650 6871 Grasslands 0.2028 Æ 0.0367 0.2356 Æ 0.0384 Woodlands Sand dunes Teiidae Aspidoscelis marmorata 69 98 2.2 1–2† 8† Generalist: 1012 508 Woodlands 0.0171 Æ 0.0114 0.0174 Æ 0.0128 Grassland Sand dunes Aspidoscelis sexlineata 54 81 2.9 1–2‡ 4† Generalist: 168 90 Grasslands 0.0031 Æ 0.0011 0.0031 Æ 0.0008 Deserts Scincidae Plestiodon obsoletus 77 130† 12.3 0–1‡ 8† Generalist: 3 2 Grasslands 0.0001 Æ 0.0002 0.00007 Æ 0.0001 Riparian Woodlands Notes: SVL, snout-vent length; SD, standard deviation. Size at maturity, maximum size, and life span for females were estimated for the populations in our study area from our data unless otherwise indicated by symbols. † Degenhardt et al. (1996). ‡ Jones and Lovich (2009). § Dietary Specialist. community that may be impacted by fragmenta- lizards throughout the ecosystem (Ryberg and tion (Leavitt and Fitzgerald 2013). Fitzgerald 2016). In fragmented areas, commu- Several studies have addressed the effects of nity structure is random compared to the nested landscape or habitat fragmentation on commu- structure of lizard communities in unfragmented nity composition, species presence, and gene areas (Leavitt and Fitzgerald 2013). Although flow (Driscoll 2004, Hoehn et al. 2007, Munguia- these studies provide important information on Vega et al. 2013). In some cases, fragmentation effects of fragmentation on community structure, per se did not affect most species (Schutz and we are not aware of any studies that have quanti- Driscoll 2008); other studies concluded fragmen- fied the effects of fragmentation on the demo- tation appeared to drive species loss and changes graphic structure of multiple lizard species in a in abundance (Driscoll 2004, Russildi et al. 2016). community. Species loss can lead to disassembly of structured Here, we evaluate the effects of landscape frag- communities (Leavitt and Fitzgerald 2013). In the mentation on capture rates and the demographic Mescalero-Monahans Sandhills ecosystem, there structure of species in a dune-dwelling lizard is a pattern of nested community structure in community. We predict that (1) the specialist

❖ www.esajournals.org 4 March 2017 ❖ Volume 8(3) ❖ Article e01729 WALKUP ET AL. species will have lower capture rates in frag- grids were 164 m apart, and the closest unfrag- mented areas, while generalist species capture mented grids were 193 m apart. All other frag- rates will be similar across fragmented and mented grids were >235 m apart, while all other unfragmented areas; (2) the demographic struc- unfragmented grids were >244 m apart. The near- ture of the endemic specialist in fragmented est fragmented grid to an unfragmented grid was areas will deviate strongly from that in unfrag- 806 m. All the trapping grids were located in mented (control) areas; and (3) the demographic shinnery oak dunes with blowouts that were structure of generalist species will show no effect known to be occupied by S. arenicolus (Laurencio of fragmentation. This is the first empirical study and Fitzgerald 2010). By design, the 27 indepen- we are aware of that describes and quantifies the dent sites were similar in landscape characteris- demographic effects of fragmentation in a com- tics. The shinnery oak dune habitat that is munity of lizards. This work provides important required by S. arenicolus was similar among all insights into how landscape fragmentation dis- trapping grids regardless of their spatial distribu- rupts population structure of ecological specialist tion and distances among them. This design species, and how species in ecological communi- allowed for statistically independent capture data, ties vary in their response to fragmentation. while testing for effects of landscape fragmenta- tion in replicated similar habitat patches. METHODS Each trapping grid consisted of 30 pitfall traps spaced 20 m apart in a 5 9 6 array, covering a From May 2009 to September 2013, we trapped total area of 1.2 ha. Traps were 20-L buckets bur- lizards on 27 pitfall grids in the Mescalero Sands ied with the rim level to the substrate with a ecosystem in Lea and Eddy Counties, New Mexico 0.165-m2 (16 9 16 in) plywood cover. Sampling (Fig. 1). Nine grids were located in areas classified took place from May to August in 2009, from as fragmented treatments, while another 18 grids April to August in 2010, and from April to were located in unfragmented areas as controls. September in 2011–2013. Trapping grids were Landscapes were classified as fragmented if there opened in four-day sessions. Each grid was were 13 or more oil well pads in a section (259 ha), opened for three sessions in 2009, and six ses- based on prior research that demonstrated a nega- sions each in 2010 through 2013. This yielded a tive correlation between lizard densities and oil total of 9720 trap-days in 2009 and 19,440 trap- well density (Sias and Snell 1998, Leavitt 2012, days each season during 2010–2013. Leavitt and Fitzgerald 2013). We selected this crite- For each lizard captured, we recorded species, rion for fragmentation because the value of 13 well trap number, sex, snout-vent length (SVL), and pads per section has become implemented as a assigned a unique permanent mark by toe-clip- management threshold for conservation of Scelo- ping. We classified individuals as adult male, porus arenicolus (Leavitt and Fitzgerald 2013). Well adult female, or juvenile based on sex and densities where the 18 unfragmented grids were reported either the minimum SVL at reproduc- located ranged from 0 to 12.95 well pads/section, tive maturity for each species or the smallest and from 31.08 to 64.75 well pads/section in recorded gravid female in our data set (which- fragmented treatments. The network of roads con- ever was smaller; Table 1). necting well pads creates a grid-like pattern of To calculate capture rates (captures/trap-day), fragmentation (Fig. 1b). Fragmentation can cause species captures were standardized by trap-days habitat degradation as well as loss of connectivity. and stratified by treatment and year. Standardiz- Across sites in the Mescalero Sands ecosystem, the ing by capture rate controlled for differences in the quality and quantity of shinnery dune habitat number of trapping grids in unfragmented and were significantly correlated (Smolensky and fragmented sites. Although lizards were individu- Fitzgerald 2011). Previous work also showed that ally marked, we had very few captures on frag- fragmented sites had fewer, smaller, and more dis- mented grids for some species (Table 1), and did persed dune blowouts than unfragmented sites not have enough recaptures on fragmented grids (Leavitt and Fitzgerald 2013). to use capture–mark–recapture methods to test for Pairwise distances among trapping grids ran- differences in population abundance in unfrag- ged from 164 to 19,054 m. The closest fragmented mented and fragmented sites. Thus, we assumed

❖ www.esajournals.org 5 March 2017 ❖ Volume 8(3) ❖ Article e01729 WALKUP ET AL. that any difference in captures was dependent Plestiodon obsoletus (Great Plains skink) from sta- only on trapping effort, and used capture rates as tistical analyses because of very few captures of a proxy for abundance. We tested for differences these species (Table 1). in mean capture rates by treatment and year for We observed statistically significant differences each species separately using two-way ANOVA. in annual mean capture rates in unfragmented The arcsine transformation reduced heteroscedas- and fragmented treatments for U. stansburiana = < = ticity and was appropriate given our question and (F1,125 9.77, P 0.01), S. arenicolus (F1,125 < = the simple arrangement of yearly capture rates 111.91, P 0.01), and H. maculata (F1,125 25.70, among treatments (Zar 1999). Significant interac- P < 0.01; Fig. 2). Sceloporus arenicolus and H. mac- tion between treatment and year indicated ulata were captured significantly more in unfrag- whether species responded to annual environmen- mented areas (unfragmented mean = 0.015, tal variability similarly in both treatments. standard deviation [SD] = 0.020; fragmented Monthly captures were pooled across years mean = 0.001, SD = 0.001, unfragmented mean = for each demographic, and then contingency 0.005, SD = 0.004; fragmented mean = 0.001, tables were used to test the hypothesis of no dif- SD = 0.002, respectively). Captures of the special- ference in demographic structure of each species ist S. arenicolus were remarkably low in the between fragmented and unfragmented treat- fragmented areas, with only 31 of 1421 captures ments (Fitzgerald et al. 1999). We assumed that from five of the nine fragmented grids (range the frequencies of captures of each demographic 1–11 individuals captured on each fragmented on unfragmented sites represented the baseline grid). We did not capture S. arenicolus on four of demographic structure of the lizard populations the nine fragmented grids in five years of trap- in this ecosystem. Based on that assumption, we ping, despite deliberate placement of grids in calculated the expected frequencies for captures close proximity to recent museum records of of each demographic on fragmented grids, using S. arenicolus. The generalist species, U. stansburi- the observed frequencies on unfragmented sites. ana, had higher capture rates in fragmented areas Those expected frequencies were then tested (fragmented mean = 0.24, SD = 0.04; unfrag- against observed frequencies for the fragmented mented mean = 0.20, SD = 0.04). There were no sites for the contingency tables. For Uta stansburi- differences in mean capture rates for A. mar- ana (common side-blotched lizard) and Aspidoscelis morata, A. sexlineata,andS. consobrinus between = = = marmorata (marbled whiptail), we subdivided the treatments (F1, 125 0.14, P 0.71, F1, 125 1.04, = = = contingency tables and performed chi-square tests P 0.31, F1, 125 0.96, P 0.33, respectively). for differences in monthly proportions of each Capture rates varied significantly across years = < demographic on fragmented grids; the other spe- for U. stansburiana (F4,125 36.47, P 0.01), = < cies had such low frequencies (multiple cells with S. arenicolus (F4,125 6.23, P 0.01), H. maculata = < = less than two expected captures) on fragmented (F4,125 5.89, P 0.01), A. sexlineata (F4,125 < = grids each month that the assumptions of the 16.73, P 0.01), and S. consobrinus (F4,125 6.69, chi-square test were violated and the tests were P < 0.01; Fig. 2). The highest capture rates for not performed (Fitzgerald et al. 1999, Zar 1999). these five species occurred in 2011, while the low- est capture rates occurred in 2013 for S. arenicolus, RESULTS H. maculata, S. consobrinus,andA. sexlineata and in 2009 for U. stansburiana. Aspidoscelis marmorata From 2009 to 2013, we had a total of 22,279 capture rates did not vary significantly across = = captures of eight species of lizards. Uta stansburi- years (F4,125 1.43, P 0.23). ana was the most common (18,521 total captures), There was a significant statistical interaction followed by Aspidoscelis marmorata (1520) and between treatment (fragmented vs. unfragmented) = Sceloporus arenicolus (1421). Three species, Hol- and year for U. stansburiana (F4,125 4.36, < = = brookia maculata (common lesser earless lizard), P 0.01) and A. sexlineata (F4,125 3.24, P 0.01), Aspidoscelis sexlineata (six-lined racerunner), and revealing a pattern of inter-annual variation in Sceloporus consobrinus (prairie lizard), were cap- capture rates among unfragmented and frag- tured in much lower frequencies. We excluded mented grids (Fig. 2). Uta stansburiana capture Phrynosoma cornutum (Texas horned lizard) and rates were higher on unfragmented grids than on

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Unfragmented Fragmented 0.040 0.040

0.030 0.030

0.020 0.020 arenicolus Sceloporus 0.010 0.010

0.000 0.000 0.008 0.008

0.006 0.006

0.004 0.004 maculata

Holbrookia 0.002 0.002

0.000 0.000 0.400 0.400

0.300 0.300

0.200 0.200 Uta 0.100 0.100 stansburiana 0.000 0.000 0.028 0.028

0.021 0.021

0.014 0.014 Captures per trap-day

marmorata 0.007 0.007 Aspidoscelis

0.000 0.000 0.012 0.012

0.009 0.009

0.006 0.006

sexlineata 0.003 0.003 Aspidoscelis

0.000 0.000 0.008 0.008

0.006 0.006

0.004 0.004

Sceloporus 0.002 0.002 consobrinus

0.000 0.000 2009 2010 2011 2012 2013 2009 2010 2011 2012 2013

Fig. 2. Yearly capture rates (captures/trap-days) for each species on unfragmented and fragmented trapping grids. The scale of the y-axis is different for each species relative to their abundance. fragmented grids in 2009 and higher on frag- P = 0.25, respectively). There was also no signifi- mented grids in 2010–2013. Aspidoscelis sexlineata cant interaction for S. consobrinus and A. mar- capture rates were higher on unfragmented grids morata, species that were not dependent on dune = = in 2009, 2012, and 2013 and higher on fragmented blowout landforms (F4,125 0.84, P 0.51, and = = grids in 2010 and 2011. There was no interaction F4,125 0.72, P 0.58, respectively). between year and treatment for the specialist Tests of contingency tables identified impor- S. arenicolus, nor for H. maculata,whichwere tant differences in demographic proportions for both significantly less numerous on fragmented some species (Fig. 3). Overall for U. stansburiana, = = = fi grids (F4,125 1.19, P 0.32, and F4,125 1.38, signi cantly more juveniles and fewer adults

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Unfragmented Fragmented 225 439 320 139 178 73 5 11 2 6 6 0 1.0 0.8 0.6 0.4 Sceloporus arenicolus* 0.2 0.0 17 28 83 46 40 6 3 11 9 1 8 0 1.0 0.8 0.6 0.4 maculata Holbrookia 0.2 0.0 1364 1992 1857 2308 2233 1377 751† 1275† 890 1259 1472 898† 1.0 0.8 0.6

Uta 0.4

stansburiana* 0.2 0.0 102 223 281 203 146 34 37 191 117 74† 48† 25 1.0 0.8 0.6 Proportion of Individuals 0.4 Aspidoscelis marmorata* 0.2 0.0 64070261332312911111 1.0 0.8 0.6 0.4 sexlineata Aspidoscelis 0.2 0.0 14 55 43 29 21 6 816141146 1.0 0.8 0.6 0.4 Sceloporus consobrinus 0.2 0.0 Apr May Jun Jul Aug Sep Apr May Jun Jul Aug Sep

Juvenile Adult male Adult female

Fig. 3. Demographic structures of each species on unfragmented and fragmented trapping grids from April to September, corresponding to the active season for lizards. Bars represent the proportion of juveniles, adult males, and adult females captured each month. All five years of sampling are combined; sample sizes for each month

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(Fig. 3. Continued) are above the bars. The asterisk (Ã) next to the species name indicates that on the fragmented grids that popula- tion had significantly different overall demographic proportions than expected compared to the baseline unfrag- mented grids. The dagger (†) next to the monthly sample sizes for Uta stansburiana and Aspidoscelis marmorata indicates that on the fragmented grids that population had significantly different demographic proportions that month than expected compared to the baseline unfragmented grids.

2 were captured on fragmented grids (v = 43.91, generalist species exhibited a range of responses df = 2, P < 0.0001). Subdivided contingency tables to fragmentation. Some generalists responded revealed significantly fewer adult females and negatively, in particular Holbrookia maculata,while more juveniles were captured in April and May others appeared to prosper, namely Uta stansburi- 2 2 (v = 53.40, df = 2, P < 0.0001, and v = 79.69, ana and Aspidoscelis marmorata. A similar pattern df = 2, P < 0.0001, respectively). In September, was described by Vega et al. (2000), who showed we captured significantly larger proportions of strong reduction in habitat area and population juveniles and smaller proportions of adult males density in a habitat specialist lizard following 2 (v = 12.37, df = 2, P = 0.0021). There were no sig- construction of a road through coastal dunes and nificant differences in demographic proportions little response by the generalists. for this species in June, July, and August on frag- The endemic and threatened habitat specialist, mented sites (P > 0.05). Sceloporus arenicolus, merits careful discussion, The overall contingency table for A. marmorata because it lends insight as to how specialist spe- showed there were significantly more juveniles cies are affected by isolation and habitat degrada- and fewer adults captured on fragmented grids tion following fragmentation. Sceloporus arenicolus 2 (v = 7.18, df = 2, P = 0.0276; Fig. 3). The subdi- disappeared from fragmented sites and its demo- vided contingency table showed July had signifi- graphic structure was clearly disrupted compared cantly fewer adult males and more juveniles to unfragmented sites, where we observed a typi- 2 (v = 7.03, df = 2, P = 0.0297) and in August there cally structured sequence of demographic cohorts 2 were significantly more adult males (v = 6.64, across months during all sample years. Capture df = 2, P = 0.0362). There were no statistically sig- rates of S. arenicolus were very low on fragmented nificant differences in demographic proportions sites compared to unfragmented sites, and consis- in April, May, June, and September (P > 0.05). tently declined across the five years of trapping, The contingency table for S. arenicolus showed until we captured no S. arenicolus on any frag- there were significantly fewer adult males and mented grid in the final year of the project. Mean- 2 more juveniles on fragmented sites (v = 6.15, while, in the 18 unfragmented sites, capture rates df = 2, P = 0.0462; Fig. 3). There were no signifi- of S. arenicolus increased from 2009 to 2011 and cant differences in demographics for H. maculata, then decreased from 2011 to 2013, a pattern that S. consobrinus,andA. sexlineata on fragmented was not statistically significant and was not 2 and unfragmented grids (v = 1.25, df = 2, unexpected for healthy fluctuating populations. 2 P = 0.5353; v = 0.79, df = 2, P = 0.6737; and There was at least one demographic life stage 2 v = 0.34, df = 2, P = 0.8437, respectively). (adult males, adult females, or juveniles) missing each month overall, and in each of the five sea- DISCUSSION sons of the study. The demographic structure was skewed toward females on fragmented grids, Our results strongly supported our predictions albeit with few captures. We did not capture and those of Andren et al. (1997) and Henle et al. adults later in the trapping periods, with males (2004) that species with the strongest habitat pref- captured only during April through June, and erences should show the greatest response to females captured in April, May, and July. Young- landscape fragmentation. While the habitat spe- of-year were not captured during April to May on cialist was strongly affected by fragmentation, fragmented sites, so it is reasonable to assume with negative consequences for both abundance juveniles from the prior reproductive season on and demographic structure, we also showed fragmented sites either emigrated or died. While

❖ www.esajournals.org 9 March 2017 ❖ Volume 8(3) ❖ Article e01729 WALKUP ET AL. low numbers on the fragmented grids could play to the environment among years in this abun- some role in our ability to accurately assess demo- dant, short-lived generalist varied locally and graphic structure of S. arenicolus, we are confi- were not strongly influenced by fragmentation. dent, given the five years of intensive trapping, On the fragmented grids, there were more juve- these results strongly suggest this specialist spe- niles captured than expected in April, May, and cies has a relatively high susceptibility to local September with all years combined. extinction following fragmentation. Taken Aspidoscelis marmorata capture rates were con- together, we interpret these results to mean there sistent across treatments and showed no effect of were too few S. arenicolus on fragmented grids inter-annual variation. This species is longer- necessary to maintain the demographic structure lived than the other generalist species, uses many of a self-sustaining population (Figs. 2, 3). habitats, and is also the most wide-ranging, We also documented significantly fewer cap- active forager in this lizard community. Despite tures and disrupted demographic structure in the generalist nature of A. marmorata, contin- H. maculata in the fragmented sites, indicating the gency tests revealed juveniles were captured at changed landscape of the fragmented treatments significantly higher frequencies than expected on had a detrimental effect on their populations. For fragmented grids in July and August. These dif- example, on fragmented grids, only males were ferences later in the breeding season may have captured in July, where we expected to capture resulted from either more nesting in the frag- adult females and hatchlings as well. Also, we cap- mented areas or hatchlings having higher sur- tured no H. maculata in September on fragmented vival rates in fragmented areas. grids despite having captured them on unfrag- Two generalists, Sceloporus consobrinus and Aspi- mentedgridsduringthismonth.Inthisecosys- doscelis sexlineata, both with relatively moderate tem, H. maculata occurs along roads, basks on life spans, moderate body sizes, and moderate to roads, and uses several vegetation types in sandy high fecundity, showed no significant differences areas (Degenhardt et al. 1996). It remains unclear in the demographic structure at unfragmented why this species should be susceptible to fragmen- and fragmented sites. In addition, S. consobrinus tation. Leavitt and Fitzgerald (2013) examined the showed no significant response in capture rates effects of changes in habitat structure on commu- by year or treatment. The lack of response by this nity structure in this system and also found species is consistent with predictions; in this area, S. arenicolus and H. maculata were sensitive to S. consobrinus tends to use only the extensive fragmentation and consistently were the first two matrix of shinnery oak flats surrounding dune species to disappear from fragmented sites. Leavitt areas. Aspidoscelis sexlineata is a wide-ranging (2012) showed the abundance of these two species active forager that occurs within and outside was not associated with the same landscape fea- dunes, similar in life history to its congener tures. Sceloporus arenicolus abundance was associ- A. marmorata. Although for A. sexlineata we found ated with steep slopes and relatively hard soils, a significant year-by-treatment interaction in cap- while H. maculata abundance was positively asso- ture rates (with higher capture rates on frag- ciated with flat slopes and relatively hard soils, mented grids in 2010–2011), there were no clear suggesting they were affected by fragmentation differences between fragmented and unfrag- for different reasons. Even though the mechanisms mented treatments. In the end, it is likely these of how these species responded to fragmentation two species, which use habitats surrounding the may have differed, their populations showed simi- dunes, were less affected by fragmentation. lar patterns of demographic disruption. The variable response seen among these five The super-abundant (18,521 captures) short- generalist species in this lizard community can be lived generalist, U. stansburiana, had both higher at least partly explained by differences in habitat capture rates and more variable demographics in affinity, breeding phenology, and life history of fragmented areas. Capture rates were higher in the species (Fitzgerald et al. 1999). For example, unfragmented grids in some years, and higher in the pattern in the demographic structure of fragmented grids in others. Our interpretation of U. stansburiana (a small, short-lived, highly fecund this significant interaction between year and phrynosomatid) reflected its breeding phenology. treatment pattern was that stochastic responses There were high proportions of juveniles in July

❖ www.esajournals.org 10 March 2017 ❖ Volume 8(3) ❖ Article e01729 WALKUP ET AL. through September after emergence of abundant patches as an inhospitable ocean (i.e., patch-isola- hatchlings, and very low proportions of juveniles tion model), but more recently a viewpoint has the next spring, as the young grew quickly to emerged that there is a continuum of matrix and adult size. In contrast, in S. consobrinus and patch-level configurations (Didham et al. 2012). In H. maculata (phrynosomatids that are larger and the case of the Mescalero-Monahans Sandhills longer-lived, with relatively high fecundity), we ecosystem, it has been demonstrated that the observed high proportions of juveniles during a extensive network of roads and well pads prolonged breeding season, which we attributed degrades the dune blowout landform, changes to their relatively high fecundity and longer life landscape configuration, and isolates patches of spans. Finally, the active-foraging teiids A. mar- shinnery oak dunes (Hibbitts et al. 2013, Leavitt morata and A. sexlineata are larger, longer-lived, and Fitzgerald 2013, Ryberg et al. 2015). As such, and slower maturing than other species in this for species like S. arenicolus that have very specific assemblage. Their life history and breeding phe- habitat requirements, the concept of the inhos- nology help explain why we observed juveniles of pitable matrix may be more relevant. Sceloporus these species throughout the activity season, as arenicolus occurs only in and around intercon- young continue to grow to adult size throughout nected blowouts in relatively large expanses of the following year. Two species whose life history shinnery oak dunes (Fitzgerald and Painter 2009, strategies were considered intermediate, S. conso- Laurencio and Fitzgerald 2010). Movements brinus and A. sexlineata,showednochangesin among disconnected patches have never been either capture rates or demographic structure in observed. This study gives insight into the mecha- fragmented sites. Finally, the two species on the nism of how fragmentation results in disruption opposite end of the life history gradients among of demographic structure in isolated populations the species we studied, U. stansburiana (short- of S. arenicolus. Previous studies of this habitat lived, habitat generalist) and A. marmorata (long- specialist showed that areas of poor dune quality lived, large, wide-ranging forager), appeared to were population sinks. Persistence in poor-quality benefit at the fragmented sites. habitat relied on diffusion dispersal of juveniles Although the effects of habitat loss and frag- through interconnected dune blowouts to offset mentation are tightly intertwined, studies that the imbalance between natality and mortality in have tried to isolate the effects of both of these sink neighborhoods (Ryberg et al. 2013). Land- landscape changes have found habitat loss gener- scape condition, which is negatively affected by ally has a stronger effect on populations than does fragmentation, and population impacts go hand- habitat fragmentation per se (Fahrig 1997). In our in-hand. There are tight linkages between condi- study system, the network-like development of tion of shinnery dune blowouts and vital rates of well pads and their connecting roads both isolates S. arenicolus; elasticities in adult survival, juvenile populations and disrupts the underlying geomor- survival, and fertility of S. arenicolus were strongly phologic processes that maintain the shinnery oak and significantly associated with fractal dimen- dune blowout formations (Ryberg et al. 2015). In sion of interconnected dune blowouts (Ryberg comparison with other drivers of fragmentation, et al. 2015). Moreover, fragmentation of the shin- such as deforestation, this road-network type nery dune landscape leads to disassembly of the of fragmentation directly converts a relatively entire lizard community, largely because of the smaller percentage of the landscape surface (e.g., loss of the habitat specialist (Leavitt and Fitzger- Smolensky and Fitzgerald 2011), but drives ald 2013). The incredibly low capture rates we processes that result in large-scale degradation of observed in isolated fragmented sites compared irreplaceable landforms on which the habitat to unfragmented sites over five years reflect the specialist depends (Ryberg et al. 2015). Accord- disruption of demographic structure in popula- ingly, we believe the disrupted demography and tions that have become isolated with no rescue declines observed in S. arenicolus and H. maculata effect from immigration. The end result for small, were driven by the effect of fragmentation on isolated populations of S. arenicolus is localized landscape integrity and habitat quality. extinctions. Fragmentation theory has previously treated This study also lends insight into the linkages the matrix of vegetation that lies between habitat between disturbance of landscape features and

❖ www.esajournals.org 11 March 2017 ❖ Volume 8(3) ❖ Article e01729 WALKUP ET AL. the consequences for populations. In short, frag- LITERATURE CITED mentation disrupts both the landscape features and the lizard populations. This is the first study Alcala, A. C., and W. C. Brown. 1967. Population ecol- to link empirically derived patterns of demo- ogy of the tropical scincoid lizard, Emoia atrocostata, in the Philippines. Copeia 1967:596–604. graphic structure to landscape fragmentation in a lizard community that contains specialist and Andren, H., A. Delin, and A. Seiler. 1997. Population response to landscape changes depends on special- generalist species. We were able to make direct ization to different landscape elements. Oikos 80: comparisons of population structure at unfrag- 193–196. mented and fragmented sites, and we demon- Attum, O., P. Eason, G. Cobbs, and S. M. Baha El Din. strated deterioration of demographic structure 2006. Response of a desert lizard community to could be a sign of impending extirpation of spe- habitat degradation: Do ideas about habitat spe- cies affected by fragmentation. As such, this cialists/generalists hold? Biological Conservation study enhances previous work on the effects of 133:52–62. fragmentation on this lizard community, and Ballinger, R. E. 1973. Comparative demography of two demonstrates how populations that are sensitive viviparous iguanid lizards (Sceloporus jarrovi and – to fragmentation may begin to deteriorate Sceloporus poinsetti). Ecology 54:269 283. through the loss of specific components (adult Barbault, R., and Y. Mou. 1988. Population dynamics of the common wall lizard, Podarcis muralis,in males, adult females, or juveniles) of their popu- southwestern France. Herpetologica 44:38–47. lation structure. Future work could build on the Bellard, C., C. Leclerc, B. Leroy, M. Bakkenes, S. Veloz, relationships we have drawn between life history W. Thuiller, and F. Courchamp. 2014. Vulnerability traits and habitat affinity of species, and how of biodiversity hotspots to global change. Global these may serve as predictors of how species Ecology and Biogeography 23:1376–1386. may respond to fragmentation. This research Betts, M. G., L. Fahrig, A. S. Hadley, K. E. Halstead, enhances the picture of how fragmentation may J. Bowman, W. D. Robinson, J. A. Wiens, and D. B. cause demographic disruption and decline of Lindenmayer. 2014. A species-centered approach some species while having little effect on others. for uncovering generalities in organism responses to habitat loss and fragmentation. Ecography 37: 517–527. ACKNOWLEDGMENTS Brooks, T. M., et al. 2002. Habitat loss and extinction in the hotspots of biodiversity. Conservation Biol- Field work could not have been accomplished with- ogy 16:909–923. out the following field assistants: Matthew Acre, Curt Bustard, H. R. 1969. The population ecology of the Barnes, Levi Cole, Kevin Creely, Drew Dittmer, Austin gekkonid lizard (Gehyra variegata (Dumeril & Fitzgerald, Timothy Gibble, Johanna Harvey, Allison Bibron)) in exploited forests in northern New Leavitt, Kevin Narum, Anthony Romano, Brian Romm, South Wales. Journal of Ecology 38: and Christopher Schalk (Texas A&M). Debra Hill and 35–51. Ty Allen (US DOI: USFWS) had a crucial role in estab- Caswell, H. 2001. Matrix population models. Second lishing and implementing this research in 2009. We edition. Sinauer, Sunderland, Massachusetts, thank Bill and Linda Gideon for all their support in the USA. community of Maljamar. We thank Charles W. Painter Degenhardt, W. G., C. W. Painter, and A. H. Price. for his unflagging support and help. This research was 1996. Amphibians and of New Mexico. supported by the Department of the Inte- University of New Mexico Press, Albuquerque, rior: Bureau of Land Management, received research New Mexico, USA. approval from the NMDGF (permit: 3409 SCI), and fol- Devictor, V., R. Julliard, and F. Jiguet. 2008. Distribu- lows the institutional animal use protocols under the tion of specialist and generalist species along following Texas A&M University approval: AUP no. spatial gradients of habitat disturbance and frag- 2008-95. A contribution to open access publishing fees mentation. Oikos 117:507–514. for this article was provided by the Texas A&M Univer- Didham, R. K., V. Kapos, and R. M. Ewers. 2012. sity Open Access to Knowledge Fund (OAKFund), sup- Rethinking the conceptual foundations of habitat ported by the University Libraries and the Office of the fragmentation research. Oikos 121:161–170. Vice President for Research. This is publication number Dirzo, R., and P. H. Raven. 2003. Global state of bio- 1541 from the Biodiversity Teaching and Research diversity and loss. Annual Review of Environment Collections. and Resources 28:137–167.

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