Bird assemblage structure in the Desert Puna in areas with different disturbance activity of a subterranean herbivorous rodent

2.1. Study area

This study was conducted in Don Carmelo Multiple Use Private Reserve, a protected area of about 44,000 ha, located in La Invernada valley (31° 10’S, 69° 46’ W), in San Juan province, Argentina (Figure 1). The study area is located in the southernmost extent of the Puna ecoregion, a desert environment at an elevation of > 3,100 m (Ellenberg, 1979Ellenberg, H., 1979. Man’s influence on tropical mountain ecosystems in South America. Journal of Ecology, 67: 401-416. 10.2307/2259105; Matteucci, 2012Matteucci, S., 2012. Ecorregión Puna. In: J. Morello, S.D. Matteucci, A.F. Rodríguez & M. Silva (eds.), Ecorregiones y Complejos Ecosistémicos Argentinos. Buenos Aires, Argentina: Orientación Gráfica SRL. 87-127 pp.). Vegetation is composed of low xerophytic shrubs and grasses (i.e., a shrub-steppe environment), with a large amount of bare soil (Márquez, 1999Márquez, J. 1999. Las áreas protegidas de la Provincia de San Juan. Multequina, 8: 1–10.; Lara et al., 2007Lara, N., Sassi, P., & Borghi, C.E., 2007. Effect of herbivory and disturbances by tuco-tucos (Ctenomys mendocinus) on a plant community in the southern Puna Desert. Arctic, Antarctic, and Alpine Research, 39: 110–116. 10.1657/1523-0430(2007)39[110:EOHADB]2.0.CO;2; Ripoll & Martínez Carretero, 2019Ripoll, Y., & Martinez Carretero, E., 2019. Vegetación del Valle la Invernada (Reserva Privada Don Carmelo) en el Centro Oeste de la Provincia de San Juan (Argentina). Boletín de la Sociedad Argentina de Botánica, 54: 405-419. 10.31055/1851.2372.v54.n2.25370). The climate of Puna at this latitude is dry, cold, with a wide daily temperature range, and primarily summer rainfall. The mean annual temperature is 8.15 °C, maximum absolute temperature is 26 °C, and minimum absolute temperature is -22 °C. Precipitation is about 100 mm/year, and snowfall occurs mainly between May and October with thickness up to 50 cm. Snow usually remains on the ground for no longer than 15 days (Andino & Borghi, 2017Andino, N., & Borghi, C.E., 2017. Occurrence of Ctenomys mendocinus in a high-altitude cold desert: effect on density, biomass, and fitness of sagebrush plants. Arctic, Antarctic, and Alpine Research, 49: 53–60. 10.1657/AAAR0015-061).

Figure 1. Location of the study area at the Don Carmelo Multiple Use Private Reserve in the south of Puna, San Juan Province, Argentina. Legend: a) Location of Argentina (in gray) within South America; b) Detail of the location of the Reserve (in gray) in the province of San Juan (Argentina); c) Reserve delimited by a continuous black line showing the study area in gray; d) Detail of Don Carmelo Multiple Use Private Reserve delimited by a continuous black line showing the study area in gray. 

Figura 1. Ubicación del área de estudio en la Reserva Privada de Usos Múltiples Don Carmelo, en el sur de la Puna, provincia de San Juan, Argentina. Leyenda: a) Ubicación de Argentina (en gris) dentro de Sudamérica; b) Detalle de la ubicación de la Reserva (en gris) en la provincia de San Juan (Argentina); c) Reserva delimitada por una línea continua negra que muestra el área de estudio en gris; d) Detalle de la Reserva Privada de Usos Múltiples Don Carmelo delimitada por una línea continua negra que muestra el área de estudio en gris. 

The most abundant herbivores occurring in the reserve are guanacos (Lama guanicoe) and the subterranean rodent Ctenomys mendocinus, locally called tuco-tuco. C. mendocinus are subterranean hystricognath rodents with a mass of 108-253 g, that dwell in areas ranging from 400 m to 3,200 m.a.s.l. in arid and semi-arid environments of western Argentina (Rosi et al., 2005Rosi, M.I., Cona, M., Roig, V.G., Massarini, A.I., & Verzi, D.H., 2005. Ctenomys mendocinus. Mammalian Species, 777: 1–6. 10.1644/777.1). C. mendocinus are strict herbivores, primarily consuming woody plants, but also feeding on grasses when available (Rosi et al., 2003Rosi, M.I., Cona, M.I., Videla, F., Puig, S., Monge, S.A., & Roig, V.G., 2003. Diet selection by the fossorial rodent Ctenomys mendocinus inhabiting an environment with low food availability (Mendoza, Argentina). Studies on Neotropical Fauna and Environment, 38: 159–166. 10.1076/snfe.38.3.159.28168), creating discrete patches through their intense herbivory, characterized by an increase in bare soil cover and a decrease in grass and shrub cover (Andino & Borghi, 2017Andino, N., & Borghi, C.E., 2017. Occurrence of Ctenomys mendocinus in a high-altitude cold desert: effect on density, biomass, and fitness of sagebrush plants. Arctic, Antarctic, and Alpine Research, 49: 53–60. 10.1657/AAAR0015-061, Borghi et al. 2020Borghi, C.E., Rodríguez Navas, A., & Andino, N., 2020. A subterranean ecosystem-engineering rodent influences plant emergence and reproductive strategy in a high-altitude cold desert. Journal of Mammalogy, 101: 1601-1608. 10.1093/jmammal/gyaa118) (Figure 2). The area of these disturbed patches ranges from around 700 to 20,000 m². C. mendocinus home range depends on sex and locality, ranging from 12 to 43 m² (Rosi et al., 2005Rosi, M.I., Cona, M., Roig, V.G., Massarini, A.I., & Verzi, D.H., 2005. Ctenomys mendocinus. Mammalian Species, 777: 1–6. 10.1644/777.1). In Don Carmelo Multiple Use Private Reserve, density of tuco-tucos ranges from 3.3 to 11.7 / ha (Borruel, 2013Borruel, N. 2013. Efectos en cascada (directa e inversa) de Ctenomys sobre las comunidades de reptiles (Squamata) y artrópodos (Aracnidae e Insecta) en el sur de la Puna. Doctoral Thesis, Universidad Nacional de Córdoba, Argentina.), with this burrowing activity also affecting soil nutrient concentration (Lara et al., 2007Lara, N., Sassi, P., & Borghi, C.E., 2007. Effect of herbivory and disturbances by tuco-tucos (Ctenomys mendocinus) on a plant community in the southern Puna Desert. Arctic, Antarctic, and Alpine Research, 39: 110–116. 10.1657/1523-0430(2007)39[110:EOHADB]2.0.CO;2).

Figure 2. Photos of Ctenomys mendocinus and its effect in the Don Carmelo Multiple Use Private Reserve landscape. a) Close-up of a C. mendocinus emerging from its burrow. b) Landscape with a C. mendocinus, illustrating the animal in its broader ecological context. c) Detail ofLycium chanar branches diagonally cut by the foraging activity of C. mendocinus. The distinct beveled cuts indicate the species' characteristic feeding method, underlining its influence on local flora. d) New C. mendocinus surface activity: a view of an area with two mounds of soil. e) Less disturbed habitat, offering a visual contrast to areas with higher levels of disturbance from C. mendocinus activity. f) Area heavily disturbed by C. mendocinus activity, showing the changes in the landscape resulting from their activity. 

Figura 2. Fotos de Ctenomys mendocinus y su efecto en la Reserva Privada de Uso Múltiple Don Carmelo. a) Primer plano de un C. mendocinus emergiendo de su cueva. b) Paisaje con un C. mendocinus, mostrando al animal en su contexto ecológico. c) Detalle de ramas de Lycium chanar cortadas a bisel por C. mendocinus. Los cortes biselados son distintivos de la especie. d) Nueva actividad superficial de C. mendocinus: vista de un área con dos montículos de suelo. e) Hábitat menos afectado, ofreciendo un contraste visual con áreas de mayor perturbación por la actividad de C. mendocinus. f) Área fuertemente alterada por la actividad de C. mendocinus, mostrando los cambios en el paisaje resultantes de su actividad. 

The study site was located on a high-altitude plateau, situated between the north-south oriented Sierra del Tigre and Sierra de la Invernada mountain ranges. Spanning approximately 4 km in width (west to east) and 15 km in length (north to south), this plateau maintains a consistent elevation ranging from 3,000 to 3,100 m.a.s.l. Such uniformity ensures comparable climatic and environmental conditions across all sampled transects, providing a stable context for our study. Within this expanse, patches are found in various states of disturbance ranging from very old patches, where vegetation is in the process of recovering, to patches where disturbance activity by tuco-tucos has been very recent. For this study, we selected only those patches that were either highly disturbed (but not in a recovery process) or relatively undisturbed (undisturbed) by C. mendocinus. In the disturbed patches, the abundance of burrow holes was approximately 9.6 times greater than in the undisturbed ones, soil mounds were about 7.4 times more prevalent, and plant cover was 55 % less than in undisturbed patches (Table 1).

2.2. Field methods

Fieldwork was conducted from February 2001 to October 2004. In February 2001, sampling was carried out to characterize the plant cover, as well as to quantify the abundance of mounds and burrow holes created by Ctenomys mendocinus. This sampling was performed across two distinct types of areas: those heavily disturbed (disturbed) by the activities of C. mendocinus and those that remained relatively undisturbed (undisturbed). The degree of disturbance by C. mendocinus on the vegetation was assessed visually, ensuring consistency in our categorization of each patch. To accurately describe this influence, we randomly established thirty transects, each measuring 30 m in length, across both disturbed and undisturbed sites. Specifically, fifteen transects were placed in areas heavily disturbed by tuco-tucos, and fifteen were situated in relatively undisturbed patches (Figure 2). For each transect, we collected samples from ten plots, each covering an area of 2 m² and spaced 1 m apart, resulting in a total sampled area of 20 m² per transect. The sampling unit was the transect.

To assess the influence of Ctenomys mendocinus on bird populations, fieldwork was conducted from February 2003 through October 2004. We selected two types of patches: (1) patches highly disturbed by tuco-tucos (with high density of holes [1.73 ± 0.11 /m², mean ± SE] and mounds [0.91 ± 0.03 /m²];= ‘‘disturbed patches’’), and (2) patches relatively undisturbed by Ctenomys (with low density of holes [0.18 ± 0.05 /m²] and mounds [0.12 / ± 0.02 / m²]; = ‘‘undisturbed patches’’) Lara et al. (2007Lara, N., Sassi, P., & Borghi, C.E., 2007. Effect of herbivory and disturbances by tuco-tucos (Ctenomys mendocinus) on a plant community in the southern Puna Desert. Arctic, Antarctic, and Alpine Research, 39: 110–116. 10.1657/1523-0430(2007)39[110:EOHADB]2.0.CO;2). We randomly selected 109 patches (with a diameter of 50 meters or larger) for this purpose, divided between disturbed (56) and undisturbed (53), ensuring each patch was represented by a single transect. These transects, 50 m in length and 40 m in width, were placed at least 200 m apart to minimize overlap in bird territories. Surveys were carried out during times of peak bird activity – in the early morning (7:30 am to 10:30 am) and late afternoon (4:30 pm to 7:30 pm) – across three seasons: summer (February 2003), autumn (May 2003), and spring (October 2004). Each transect was walked at a steady pace for 30 minutes by the same observer, who recorded sightings of bird species, identified with the help of the field guide by Narosky and Yzurieta (2003Narosky, T, & Yzurieta, D., 2003. Birds of Argentina and Uruguay. Identification Guide - A Field Guide. (16ª ed). Buenos Aires, Argentina: Vázquez Mazzini Editores.). The scientific and common names of the birds observed are listed in Table 2.

2.3 Data analysis

To describe and assess the ecological effect of Ctenomys activity on plant cover, burrow openings, and soil mounds, we employed Generalized Linear Models (GLMs) with appropriate error distributions for each type of data. Gaussian error distribution was used for the continuous variable of plant cover, whereas a negative binomial distribution was employed for the count data of burrow holes and soil mounds to accommodate overdispersion. We incorporated disturbance level as a fixed effect in all models to directly evaluate its ecological effect. The statistical analyses were performed in R (R Core Team, 2021R Core Team. 2021. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.), utilizing the functions ‘glm’ for Gaussian models and ‘glm.nb’ for negative binomial models, provided by the ‘stats’ and ‘MASS’ packages (Venables & Ripley, 2002Venables, W.N. & Ripley, B.D. 2002. Modern Applied Statistics with S. Fourth Edition. New York, USA: Springer.), respectively. Overdispersion was evaluated using the ‘dispersiontest’ function from the ‘AER’ package (Kleiber & Zeileis, 2008Kleiber, C., & ZeileisA. 2008. Applied econometrics with R. New York, USA: Springer.). Additionally, we employed the ‘emmeans’ package to estimate and interpret the fixed effects with their confidence intervals, thereby quantifying the magnitude of disturbance’s influence.

We applied Generalized Linear Mixed Models (GLMMs; Zuur et al., 2009Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., & Smith, G.M., 2009. Mixed effects models and extension in ecology with R. New York, USA: Springer. 10.1007/978-0-387-87458-6) with Poisson error distribution and Negative Binomial error distribution if variables exhibited overdispersion (Ĉ > 1; Crawley, 2007Crawley, M.J., 2007. The R book. London, England: John Wiley and Sons.) to analyze if C. mendocinus disturbance affects the abundance of all bird species occurring in the area. The response variable was abundance of all bird species, the explanatory variable was disturbance by Ctenomys (two levels: disturbed and undisturbed patches), and the random effect used was the month of survey (three levels: February, May and October). GLMMs were fitted using the glmer function from the lme4 package (Bates et al., 2015Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67: 1–48. 10.18637/jss.v067.i01). The significance of fixed and random effects was assessed using the likelihood ratio test (LRT; Bolker et al., 2008Bolker, B., Brooks, M., Clark, C., Geange, S., Poulsen, J., Stevens, H., & White, J., 2008. General linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution, 24: 127–135. 10.1016/j.tree.2008.10.008).

To determine the impact of Ctenomys disturbances on avian populations, we concentrated on species with total abundances greater than 20 individuals, analyzing data from months with significant recorded abundances. This approach aimed to enhance the statistical robustness of our intra-specific abundance comparisons, focusing on the effects of disturbances on four bird species: Oreopholus ruficollis and Thinocorus rumicivorus in February, and Muscisaxicola cinereus along with Geositta cunicularia in May. We encountered significant numbers of zero counts in our bird species abundance data, exceeding what standard Poisson or Negative Binomial distributions would predict, indicative of excess zeros. The data also exhibited over-dispersion, where variance surpassed the mean, suggesting that these standard models were insufficient for our analysis (Zuur et al., 2012Zuur, A, Saveliev, A., Ieno, E.N., 2012. Zero Inflated Models and Generalized Linear Mixed Models with R. Highland Statistics Ltd.). To accurately assess the effect of Ctenomys disturbances, we employed Zero-Inflated models, which are adept at managing datasets characterized by excess zeros and over-dispersion. These models include two components: a logistic regression model that predicts the likelihood of zero counts, and a count model (Poisson or Negative Binomial) for the positive counts. Depending on the dispersion index (Ĉ > 1; Crawley, 2007Crawley, M.J., 2007. The R book. London, England: John Wiley and Sons.), we applied Zero-Inflated Poisson Models (ZIP) and Zero-Inflated Negative Binomial Models (ZINB) using the pscl package (Jackman, 2020Jackman, S. 2020. pscl: Classes and Methods for R Developed in the Political Science Computational Laboratory. United States Studies Centre, University of Sydney. Sydney, Australia. R package version 1.5.5. URL https://github.com/atahk/pscl/) and the lmtest package (Zeileis & Hothorn, 2002Zeileis, A., & T. Hothorn, 2002. Diagnostic Checking in Regression Relationships. R News2(3): 7–10.). The significance of the disturbance effect as a fixed effect in our models was evaluated using the likelihood ratio test (LRT; Bolker et al., 2008Bolker, B., Brooks, M., Clark, C., Geange, S., Poulsen, J., Stevens, H., & White, J., 2008. General linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution, 24: 127–135. 10.1016/j.tree.2008.10.008), enabling us to discern the effect of Ctenomys disturbances on bird species abundance.

To evaluate the differences in bird species richness and diversity in areas with varying levels of C. mendocinus activity, as well as to analyze the variations in the rank-abundance curves among these areas, we adopted a comprehensive analytical approach. We analyzed the entire dataset, incorporating all species recorded throughout the study period without omitting any due to low abundance. This comprehensive dataset underpinned the calculation of diversity indices, such as species richness, Shannon diversity, and Simpson diversity. Our approach ensured that the resultant diversity indices accurately reflect the full ecological complexity of both disturbed and undisturbed sites, without bias from species omission. As every patch type (disturbed by Ctenomys and undisturbed) had a different number of transects (56 and 53 respectively), we performed coverage-based rarefaction curves to estimate sampling completeness at each patch type (Chao et al., 2014Chao, A., Gotteli, N., Hsieh, T., Sander, E., Ma, K., Colwell, R, & Ellison, A., 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs, 84: 45-67. 10.1890/13-0133.1). Sample completeness refers to the proportion of total abundance or number of individuals in an assemblage that belong to the species represented in the sample (Chao & Jost, 2012Chao, A., & Jost, L., 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93: 2533-2547. 10.1890/11-1952.1).

In order to quantify the species diversity in disturbed and undisturbed sites, ⁰D, ¹D and ²D metrics was used, which are parameterized by the Hill numbers 0, 1 and 2, respectively (Hill, 1973Hill, M. O., 1973. Diversity and evenness: a unifying notation and its consequences. Ecology, 54: 427-432. 10.2307/1934352; Jost, 2006Jost, L., 2006. Entropy and diversity. Oikos, 113: 363–375. 10.1111/j.2006.0030-1299.14714.x). The values of q are referred to as the “order” of the diversity measure. ⁰Dα represents species richness (q = 0); ¹Dα, Shannon diversity index, represents the number of common species (q = 1); and ²Dα, Simpson diversity index, represents the number of dominant species in a community (q = 2) (Jost, 2006Jost, L., 2006. Entropy and diversity. Oikos, 113: 363–375. 10.1111/j.2006.0030-1299.14714.x). We used the function mcpHill (R package “simboot”) to compare diversities of patches highly disturbed by Ctenomys and undisturbed (Pallmann et al., 2012Pallmann, P., Hothorn, L., Fischer, C., Nacke, H., Priesnitz, K., & Schork, N., 2012. Assessing group differences in biodiversity by simultaneously testing a user-defined selection of diversity indices. Molecular Ecology Resources, 12: 1068–78. 10.1111/1755-0998.12004; Scherer & Pallmann, 2017Scherer, R., & Pallmann, P., 2017. SIMBOOT: Simultaneous Inference for Diversity Indices. R package version 0.2-6. https://CRAN.R- project.org/package=simboot; Canty & Ripley 2019Canty, A., & Ripley, B., 2019. boot: Bootstrap R (S-Plus) Functions (R package version 1.3-20) [Computer software]. The Comprehensive R Archive Network.). We assessed statistical differences in species diversity by applying multiple contrast tests based on the resampling technique (Westfall & Young, 1993Westfall, P.H., & Young, S.S. 1993. Resampling-based multiple testing: Examples and methods for p -value adjustment. New York, USA: John Wiley and Sons, Inc.).

We characterized species diversity at both types of patches, building two types of integrated rarefaction and extrapolation curves (sample-size and coverage-based), with 95 % confidence intervals, obtained by a bootstrap method based on 1,000 replications using iNEXT package (Hsieh et al., 2016Hsieh, T.C., Ma, K.H., & Chao, A., 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7: 1451-156. 10.1111/2041-210X.12613). For sample-size curves, the maximum reference sample size (226 individuals) was used as a base sample size, and for coverage-based curves we standardized the samples to the maximum coverage for reference samples (100 %). Pielou’s evenness index (J) was calculated as a measure of equitability, i.e. the proportion of the diversity observed in each patch was assessed in relation to the maximum expected diversity (Magurran, 2004Magurran, A.E., 2004. Measuring biological diversity. Oxford, United Kingdom: Blackwell Publishing.). These analyses were supplemented with bird species rank abundance curves for both types of patches using the Biodiversity R package (Kindt & Kindt, 2019Kindt, R., & Kindt, M.R., 2019. Package ‘BiodiversityR’. Package for community ecology and suitability analysis, 2: 11-12.).

Results are presented as mean ± standard error (SE) and, for null hypothesis testing, statistical tests were considered significant at α < 0.05. All analyses were performed with R Software 3.6.1 (R Core Team 2019R Core Team, 2019. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.). Results are expressed as the untransformed mean ± SE.

3.1 Differences in bird abundance between areas with high and low activity of C. mendocinus

We recorded a total of 319 birds at patches disturbed and undisturbed by Ctenomys. They belong to two orders, seven families, eight genera and 11 species (Table 2).

Birds (all species) were significantly less abundant (93 individuals, mean number of birds per transect: 1.66 ± 0.93) at disturbed patches with high levels of activity by Ctenomys compared to undisturbed patches (226 individuals, 4.26 ± 0.88 birds/transect) (GLMM, LRTtest χ2 = 9.41; df = 1; p = 0.0021). We found that total abundance was also influenced by the random factor (month; p < 0.0001). The most abundant recorded bird species included the insectivores Muscisaxicola cinereus, Geositta cunicularia, Oreophollus ruficallis and the granivore Thinocorus rumicivorus. Since these species exhibited a migratory abundance pattern, we compared their abundances between disturbed and undisturbed sites during periods when their numbers were sufficient for statistical comparison. The most frequently recorded bird species was M. cinereus, with observations of 62 individuals in undisturbed patches versus 50 in disturbed patches during May. Following this species were G. cunicularia in May, and T. rumicivorus and O. ruficallis in February, with each species’ populations exceeding 19 individuals in a given month. The abundance of M. cinereus and T. rumicivorus was significantly different between undisturbed and disturbed patches by Ctenomys, but not that of O. ruficallis or G. cunicularia (Table 3). M. cinereus was more abundant at undisturbed than disturbed patches (mean 6.20 individuals/transect vs 3.85 respectively), and T. rumicivorus followed the same pattern (0.47 vs 0.06 respectively). Ctenomys did not affect the probability of absence of these four species (Zero-inflated models; Table 3). Mimus patagonicus, Geospizopsis plebejus, Geositta rufipennis, Asthenes dorbignyi and Sicalis auriventris were considered rare species because they were observed only in undisturbed patches and with low abundance (abundance < 4 individuals in all transects). For some cases, for instance for G. rufipennis, we observed only one individual over all study periods; and in the case of S. auriventris, we recorded three individuals just once on one transect.

3.2 Differences in bird species richness and diversity between areas with high and low activity of C. mendocinus

At undisturbed patches, we recorded 226 individuals among 11 species, and at disturbed patches we recorded 93 individuals among 6 species. Sampling completeness reached 99 % for undisturbed patches and 100 % for disturbed ones.

Using Hill numbers (i.e., the effective number of species), our evidence confirmed that undisturbed patches were significantly more diverse than those disturbed by Ctemomys (⁰D, p = 0.01; ¹D, p = 0.04; ²D, p = 0.05) (Table 4 and Figure 3). At patches undisturbed we found one species represented by one individual (singleton species) and one species represented by two individuals (doubleton species). However, at disturbed patches we did not find any singletons or doubletons. The sample-size rarefaction and extrapolation curves (base sample size= 226) showed a consistent pattern in all indexes, with the diversity curve for undisturbed patches above the curve of disturbed patches for all three parameters (Figure 3).

By standardizing both patches to the same sampling effort (sample coverage 1.00), we found that, at both types of patches, the coverage-based curves give the same ordering of diversity (⁰D > ¹D > ²D) with higher diversity at patches without disturbance than at disturbed patches (Figure 3). Pielou’s evenness shows that patches free from disturbance by Ctenomys were more similarly distributed than disturbed patches (J’ = 0.77 and J’ = 0.68, respectively).

Figure 3. Comparison of sample-size-based (left panels) and sample-coverage-based (right panels) rarefaction and extrapolation for Hill numbers: q=0 (upper panels), q=1 (middle panels), and q=2 (lower panels) for patches with herbivory by Ctenomys (circle) and without herbivory (triangle). Observed samples are denoted by solid dots; rarefied segments are denoted by solid lines and extrapolated segments by broken lines. The extrapolation extends up to a maximum sample size of 226 individuals. The sample-coverage-based extrapolation extends to the coverage value of the corresponding maximum sample size. The 95 percent confidence intervals (shaded areas) were obtained by a bootstrap method based on 1000 replications. 

Figura 3. Comparación de la rarefacción y extrapolación basadas en el tamaño de la muestra (paneles de la izquierda) y en la cobertura de la muestra (paneles de la derecha) para los números de Hill: q=0 (paneles superiores), q=1 (paneles medios) y q=2 (paneles inferiores) para parches con herbivoría por Ctenomys (círculo) y sin herbivoría (triángulo). Las muestras observadas están denotadas por puntos sólidos; los segmentos rarefactados están denotados por líneas sólidas y los segmentos extrapolados por líneas discontinuas. La extrapolación se extiende hasta un tamaño máximo de muestra de 226 individuos. La extrapolación basada en la cobertura de la muestra se extiende hasta el valor de cobertura del tamaño máximo de muestra correspondiente. Los intervalos de confianza del 95 por ciento (áreas sombreadas) se obtuvieron mediante un método de bootstrap basado en 1000 replicaciones. 

3.3 Differences in the rank-abundance curves of bird species between areas with high and low activity of C. mendocinus

The rank-abundance curve showed that Muscisaxicola cinereus was the most abundant bird species at both types of patches. At undisturbed patches, Geossita rufipennis had the lowest abundance, while Thinocorus rumicivorus had the lowest abundance at disturbed ones (Figure 4). The declining species-rank curve indicates that there is great dominance of the most abundant species at both types of patches. A. dorbingnyi was recorded only at undisturbed patches, as well as the least abundant species S. auriventris, M. patagonicus and G. rufipennis (Figure 4).

Figure 4. Rank-abundance curve for bird species recorded at patches with herbivory by Ctenomys mendocinus (dashed line), and without herbivory (solid line), at the Don Carmelo Multiple Use Private Reserve. For visualization purposes, species names are abbreviated by the first three letters of the genus and first three letters of the species epithet. Names highlighted in gray correspond to species present only at patches without herbivory. 

Figura 4. Curva de rango-abundancia para especies de aves registradas en parches con herbivoría por Ctenomys mendocinus (línea punteada), y sin herbivoría (línea continua), en la Reserva Privada de Uso Múltiple Don Carmelo. Para fines de visualización, los nombres de las especies se abrevian con las primeras tres letras del género y las primeras tres letras del epíteto de la especie. Los nombres resaltados en gris corresponden a especies presentes solo en parches sin herbivoría.