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Efficient Vs. Structured Biodiversity Inventories: Reptiles in a Mexican Dry Scrubland As a Case Study S. Trujillo–Caballero

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Efficient Vs. Structured Biodiversity Inventories: Reptiles in a Mexican Dry Scrubland As a Case Study S. Trujillo–Caballero Animal Biodiversity and Conservation 41.2 (2018) 245 Efficient vs. structured biodiversity inventories: reptiles in a Mexican dry scrubland as a case study S. Trujillo–Caballero, J. A. González–Oreja Trujillo–Caballero, S., González–Oreja, J. A., 2018. Efficient vs. structured biodiversity inventories: reptiles in a Mexican dry scrubland as a case study. Animal Biodiversity and Conservation, 41.2: 245–256, Doi: https:// doi.org/10.32800/abc.2018.41.0245 Abstract Efficient vs. structured biodiversity inventories: reptiles in a Mexican dry scrubland as a case study. Many sampling methods allow the study of species richness and diversity in biological communities, but it is not known whether a single method can determine both the number and diversity of species in an unbiased and efficient way. Here we assess whether the least biased and most efficient method to determine reptile species richness in a Mexican dry scrubland is also the best method to estimate species diversity. The lo- cal assemblage was composed of 10 species, with the Mexican mud turtle (Kinosterton integrum) and the Jalapa spiny lizard (Sceloropus jalapae) being the dominant ones. Microhabitat surveys (MHS) were the most accurate and the most efficient method to estimate species richness, but they over–estimated species diversity (+67.1 %) as much as the other sampling methods, i.e., transect surveys and pitfall–trap stations, under–esti- mated it (–59 %). Our study shows that the best sampling method to determine the number of species in local assemblages may not be the best method to study species diversity. Although combining different sampling methods can increase the project costs in terms of time, effort and money, the use of structured inventories is recommended for the analysis of species diversity. Key words: Biodiversity knowledge, Number of species, Number of equiprobable species, Sampling methods, Sampling effort, Pitman efficiency Resumen Comparación entre inventarios de biodiversidad eficientes y estructurados: los reptiles de un matorral xerófilo de México como ejemplo. Se han propuesto muchos métodos para estudiar la riqueza y la diversidad de es- pecies en comunidades biológicas, pero se desconoce si existe alguno que pueda determinar tanto el número como la diversidad de especies sin sesgo y de forma eficiente. En este estudio evaluamos si el método menos sesgado y más eficiente para determinar la riqueza de reptiles en un matorral xerófilo de México es también el mejor para estimar la diversidad de especies. La comunidad local estaba compuesta por 10 especies, de las que la tortuga de pecho quebrado y pata rugosa (Kinosterton integrum) y la lagartija escamosa jalapeña (Sceloropus jalapae) eran las dominantes. Los muestreos en microhábitats (MHS) fueron el método más exacto y eficiente para estimar la riqueza de especies, pero sobrestimaron (+67,1 %) la diversidad de especies tanto como la subestimaron (–59 %) los demás métodos (i.e., los itinerarios y las estaciones de trampas de caída). Nuestro estudio muestra que el mejor método de muestreo para determinar el número de especies en las comunidades locales tal vez no sea el mejor para estudiar la diversidad de especies. Aunque combinar diferentes métodos de muestreo puede aumentar el tiempo, el esfuerzo y los costos económicos relacionados con los proyectos, recomendamos el uso de inventarios estructurados para analizar la diversidad de especies. Palabras clave: Conocimiento de la biodiversidad, Número de especies, Número de especies equiprobables, Métodos de muestreo, Esfuerzo de muestreo, Eficiencia de Pitman Received: 17 V 17; Conditional acceptance: 19 X 17; Final acceptance: 23 X 17 Saúl Trujillo–Caballero, José Antonio González–Oreja, Facultad de Biología–BUAP, Benemérita Universidad Autónoma de Puebla, Edificio 112–A, Ciudad Universitaria, 72570 Puebla, México. Corresponding author: José Antonio González–Oreja. E–mail: [email protected] ISSN: 1578–665 X © 2018 Museu de Ciències Naturals de Barcelona eISSN: 2014–928 X 246 Trujillo–Caballero and González–Oreja Introduction timate species richness simultaneously be the best method to estimate species diversity? To the best Historically, the concept of biodiversity has been of our knowledge, this is the first time this question nearly equivalent to the number of species in a local has been posed in the biodiversity literature. In this assemblage (Sarkar, 2002; Tucker, 2005; Leitner and paper, using our data on the reptile assemblage Turner, 2013). Knowing species richness is a legiti- in a Mexican dry scrubland, we (i) compared the mate objective in ecology and conservation biology performance (in terms of bias and efficiency) of (Colwell and Coddington, 1994; Gotelli and Colwell, three sampling methods frequently used in reptile 2001; Leitner and Turner, 2013), but equality bet- biodiversity studies (Eekhout, 2010; McDiarmid et ween biodiversity and species richness is inaccurate al., 2012): microhabitat surveys, transect surveys, (Swingland, 2013). In addition to the total number and pitfall–trap stations; and (ii) analyzed whether of species, the measurement of biodiversity should the most accurate and most efficient (i.e., the best) include information about the relative importance method to estimate the number of species in our (equitability) of the species in the studied assem- local reptile assemblage was, at the same time, the blage (Gotelli and Colwell, 2011). Fortunately, the best method to study a measure of diversity that toolbox of the modern biodiversity student includes considers species equitability. many measures that consider species equitability (Magurran, 2005; Jost and González–Oreja, 2012; Gotelli and Chao, 2013). Material and methods Many factors can influence the measurement of species richness and diversity (Hill et al., 2005; Ma- Study area gurran, 2005), such as sampling effort (Colwell and Coddington, 1994; Gotelli and Colwell, 2001; Gotelli Field work was conducted at Tecali de Herrera (Pue- and Chao, 2013) and the effects that the sampling bla, Mexico: 18º 48' 24'' ‒ 18º 57' 54'' N, 97º 57' 54'' method has on the fraction of biodiversity sampled ‒ 98º 05' 42'' W), at an altitude of ca. 2,000. The (Hill et al., 2005; Sutherland, 2006; Eekhout, 2010; climate is temperate (mesothermic) and subhumid McDiarmid et al., 2012). To increase the set of truly (average values for 1951–2010: annual temperature, sampled species and to obtain a more accurate ca. 17 ºC; total annual precipitation, ca. 600 mm), estimation of the total richness, biodiversity students and rain is mostly recorded during summer (SMN, can combine (i.e., add up) data obtained with diffe- 2015). Since insolation is high and humidity is low, rent sampling methods. This practice is known as a evapotranspiration can reach elevated values (mean structured inventory (Gotelli and Ellison, 2013) and it total annual evaporation for the period 1951–2010: has frequently been applied in biodiversity studies (for 1,890 mm). Because of anthropic changes in land instance, see King and Porter, 2005; Coddington et use, most of the original vegetation has disappeared al., 2009; Gotelli et al., 2011, or Castro et al., 2017, (SEGOB, 2006) and the landscape is currently cove- for arthropods; Jenkins et al., 2003; Hutchens and red by an open, dry scrubland over diverse soil types DePerno, 2009; Sung et al., 2011; Foster, 2012;, or and geological substrates (Rzedowski, 1988; Saldaña Carpio et al., 2015, for amphibians and reptiles; or Munive, 2011). Several cacti (e.g., Echinocactus sp., Pech Canche et al., 2011, for bats). Mammillaria sp.), tree–like cacti (Stenocereus sp.), Nevertheless, because of systematic biases in and other succulent plants (like Agave salmiana, A. favor of or against certain activity periods, animal stricta, and Yucca periculosa) were dominant in this behaviors or body sizes (Hutchens and DePerno, landscape. Finally, because of the extreme climatic 2009), the different sampling methods applied in a conditions, crop fields were scarce, and several kilo- structured inventory can differ in their probability to meters away from where we completed our field work. capture different species (Yoccoz et al., 2001). As a result, differences may arise in the relative abundan- Field work ce of the registered species (Longino et al., 2002; Coddington et al., 2009) and lead to contrasting From June 2005 to April 2006, we completed monthly estimates of species diversity obtained with varied reptile inventories using the following methods sampling methods. (Latham et al., 2005; Blomberg and Shine, 2006): Reptiles are ectothermic animals, and the study (1) microhabitat surveys, (2) transect surveys, and of reptile biodiversity is not only strongly influenced (3) pitfall–trap stations. by their biology, physiology and behavior (Willmer Microhabitat surveys (MHS) are the simplest et al., 2005; McDiarmid et al., 2012; Vitt and Cald- method to capture small reptiles (Blomberg and Shine, well, 2014) but also by the environmental variables 2006). We actively searched for reptiles in sites (i.e., which constrain them (i.e., temperature or humidity; microhabitats) that are usually preferred as refuges Latham et al., 2005). All these factors can involve by the considered species (McDiarmid et al., 2012), different capture probabilities for the same species such as under rocks, fallen logs, metal sheets and the with different sampling methods (Hutchens and bark of tree trunks, or between cracks. All specimens DePerno, 2009; Rodda, 2012). Since the election were
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