Sci Nat (2016) 103: 91 DOI 10.1007/s00114-016-1416-6
ORIGINAL PAPER
Changes in behaviour and faecal glucocorticoid levels in response to increased human activities during weekends in the pin-tailed sandgrouse Fabián Casas 1,2,3 & Ana Benítez-López 2 & Rocío Tarjuelo 4 & Isabel Barja 5 & Javier Viñuela 2 & Jesús T. García 2 & Manuel B. Morales 4 & Francois Mougeot 2
Received: 2 February 2016 / Revised: 25 September 2016 / Accepted: 27 September 2016 / Published online: 11 October 2016 # Springer-Verlag Berlin Heidelberg 2016
Abstract Human recreational activities are becoming increasingly widespread and frequent, a fact that may potentially exacerbate their effects on wildlife. These human-related disturbances on animals may induce behavioural and physiological changes that can ultimately affect their fitness, showing a similar anti-predator response that against natural predator or other threats. Here, we combine the use of behavioural and physiological approaches to assess the potential effect of winter human activities on a threatened farmland bird in Europe, the pin-tailed sandgrouse (Pterocles alchata). We compared before, during and after weekend variations in human activity rates, pin-tailed sandgrouse behaviour (flocking and flying behaviour, interspecific association in mixed flocks and habitat use) and faecal glucocorticoid metabolite concentrations. Human disturbances, in particular those associated with Communicated by: Pamela C. Rasmussen
hunting activities, peaked during weekends. Sandgrouse showed significant behavioural changes (increased sandgrouse-only flock sizes, increased proportion of birds flying and changes in habitat use) during weekends and higher faecal glucocorticoid metabolite concentrations after the weekends compared with during or before weekends. Therefore, physiological stress levels could be modulated by behavioural adjustments such as increased flock sizes and changes in habitat use that may allow sandgrouse to cope with increased human disturbance rates during weekends. Nevertheless, temporal and spatial organization of hunting days among groups of estates might be good strategies to buffer these potential adverse effects on wintering pin-tailed sandgrouse and other steppe species of conservation concern, while preserving a socio-economically important activity such as hunting.
Electronic supplementary material The online version of this article (doi:10.1007/s00114-016-1416-6) contains supplementary material, which is available to authorized users.
Keywords Agricultural activities . Faecal glucocorticoid metabolites . Human leisure activities . Hunting . Mixed-species association . Pterocles alchata . Tetrax tetrax
* Fabián Casas
[email protected]
Introduction
1
Estación Experimental de Zonas Áridas (EEZA-CSIC), Carretera de Sacramento s/n, 04120 La Cañada de San Urbano, Almería, Spain
2
Instituto de Investigación en Recursos Cinegéticos (IREC, CSIC-UCLM-JCCM), Ronda de Toledo 12, 13071 Ciudad Real, Spain
3
Department of Biology, University of Maryland, College Park, MD 20742, USA
4
Terrestrial Ecology Group (TEG), Department of Ecology, Universidad Autónoma de Madrid, Madrid, Spain
5
Unidad de Zoología, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain
Human development and recreational activities (e.g. sport hunting, fishing, biking, hiking, outdoor sports, birdwatching) have steadily increased in modern societies during the last decades (Madsen and Fox 1995; Blanc et al. 2006), becoming more widespread and frequent. This fact may exacerbate their potential effect (e.g. noise and light pollution, traffic) on wildlife, involving energetically demanding changes in the distribution or behaviour of individuals (Slabbekoorn and Peet 2003; Blanc et al. 2006; Patthey et al. 2008; Steven et al. 2011; Legagneux and Ducatez 2013; Linke et al. 2013). All these changes to cope with disturbances may be induced by
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physiological responses like increased stress hormone levels (Amo et al. 2006; Thiel et al. 2008; Rehnus et al. 2014), which, if maintained over time, may have adverse effects at individual and even population levels (Wingfield et al. 1997; Ellenberg et al. 2007). The non-invasive quantification of glucocorticoid metabolite levels in faeces can improve our ability to detect disturbance effects on wild animals without disturbing or jeopardizing their safety, which is particularly important when they are threatened species (Millspaugh and Washburn 2004; Walker et al. 2005; Madliger and Love 2013). Certainly, the use of approaches based on a combination of behavioural observations and physiological stress measures would contribute to better comprehension and prediction of the responses of wild species to human activities and environmental changes (Walker et al. 2006; Cooke et al. 2014; Madliger and Love 2015). Most human outdoor leisure activities are usually concentrated during weekends (Jensen and Guthrie 2005) when animals face local-scale changes of human disturbance within a short time. Moreover, the seasonal nature of some activities, like hunting or farming (e.g. harvest, ploughing and sowing), may increase disturbance rates at certain times of the year, a critical one being winter, when environmental conditions are often harsher (Bélanger and Bédard 1989; Sastre et al. 2009). Human disturbance effects during winter have been mostly studied in wetland or upland habitats (Rees et al. 2005; Dooley et al. 2010; Thiel et al. 2011; Rehnus et al. 2014) but barely in farmland habitats (Sastre et al. 2009; Casas et al. 2009; Tarjuelo et al. 2015), although farmland species across Europe have suffered greater declines than species associated with other habitats (Donald et al. 2006). Moreover, studies combining behavioural observations and the quantification of glucocorticoid metabolite concentrations in faeces (e.g. Thiel et al. 2008; Tarjuelo et al. 2015) are particularly rare. The main human activities conducted in farmland areas during winter are hunting and agricultural activities (i.e. ploughing, sowing, olive-tree harvesting; Sastre et al. 2009). Hunting has been considered one of the main sources of disturbance for wild game animals (Madsen 1995; Madsen 1998a; Béchet et al. 2003; Duriez et al. 2005), but it can also have marked effects on the behaviour and distribution of non-target coexisting species (Madsen and Fox 1995; Casas et al. 2009; Tarjuelo et al. 2015). The pin-tailed sandgrouse (Pterocles alchata) is a steppe bird linked to open-land agricultural pseudosteppes (Martín et al. 2010b; Martín et al. 2010a; Benítez-López et al. 2014). It is highly gregarious, forming large flocks and frequently associating in mixed flocks with the little bustard (Tetrax tetrax) during winter (Martín et al. 2010a). The pin-tailed sandgrouse is currently listed as of ‘least concern’ at World and European
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levels, given its wide range and stable short-term population trend (BirdLife International 2004; BirdLife International 2015). However, in Spain, which hosts ca. 93 % of the estimated European population (Suárez et al. 2006; BirdLife International 2015), the species is currently listed as ‘vulnerable’ due to population declines and range reduction (Suárez and Herranz 2004). Overall, farmland birds are increasingly affected by human activities (Onrubia and Andrés 2005), and the pin-tailed sandgrouse seems to be particularly sensitive to anthropogenic disturbance (Mougeot et al. 2014; Benítez-López et al. 2014), although available scientific knowledge regarding this species is still scarce. Pin-tailed sandgrouse is not considered a game species in Spain since the 1980s, but sport hunting is practised in most of their distribution range, and poaching is still considered an important cause of mortality (Benítez-López et al. 2015). Therefore, hunting may have both direct and indirect effects on this species. Here, we report on the effects of human activities (hunting, farming and other leisure activities) on the behaviour and physiological stress levels of pin-tailed sandgrouse during winter, when survival is the lowest (Benítez-López et al. 2015). We quantified and compared temporal variations in human activity rates and sandgrouse behaviour (flock size, association in mixed flocks, flying frequency and habitat use) before, during and after weekends. We also examined temporal variations in sandgrouse physiological stress levels by measuring corticosterone metabolite concentrations in faeces, and further, we investigated the relationships between stress levels, disturbance rates and flocking behaviour. At present, there is little information about the utility of glucocorticoid metabolite concentrations for inferring disturbance effects during the wintering months, particularly for birds. Animals aggregating in single- or multi-species groups may obtain foraging advantages and anti-predator benefits (Galef and Giraldeau 2001; Sridhar et al. 2009). Since human disturbances may be perceived as a predatory threat, they may affect flocking behaviour through changes in group sizes or mixed-species associations (Bélanger and Bédard 1989; Mori et al. 2001). Here, we hypothesised that sandgrouse behaviour and faecal glucocorticoid metabolite concentrations would vary temporally as a response to disturbance peaks during weekends. Specifically, we expected larger sandgrouse flocks and a greater proportion of sandgrouse in mixed flocks as anti-predator responses to human disturbance, as well as a greater proportion of sandgrouse in flight, and a greater proportion of sandgrouse in habitats with greater vegetation cover that may serve as refuge. We also predicted that sandgrouse would show higher concentrations of glucocorticoid metabolites in faeces during weekends, reflecting higher levels of physiological stress associated with increased human disturbance.
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Material and methods Study area We conducted fieldwork during October 2010–January 2011 and December 2011–January 2012 (hereafter winters) in the Special Protection Area of ‘Campo de Calatrava’ (SPA 157, ca. 38° 54′ N, 3° 55′ W; central Spain), which hosts an important steppe bird community (Traba et al. 2007). This extensive farmland area (9016 ha) is primarily used for dry cereal cultivation and, secondarily, for the cultivation of leguminous crops, olive groves and vineyards. Most cereal crops are grown in a traditional 2-year rotation system (cereal/fallow rotations) that creates a landscape mosaic of sown, ploughed, stubble and fallow fields of different ages during winter (Table 1). The SPA holds a significant population of breeding (ca. 200) pin-tailed sandgrouse, which increases during autumn/winter (to ca. 1000) with the arrival of wintering birds from surrounding breeding populations (Martínez 2005; Martín et al. 2010a). Hunting is conducted in almost the entire study area (ca. 85 %) except for a few sparse fields, usually because of failed agreements with owners or their proximity ( 0.05) variables were sequentially removed from the initial models, starting with interactions. Results of the variables not included in the final model are also shown (Tables 2, 3 and 4), but level estimates were calculated only for significant variables retained in the final model. Post hoc Tukey’s HSD tests were applied when variation in response variables was explained by a categorical explanatory variable (winter, week day, daytime period or week day × daytime interaction).
Results Temporal variations in human activity rates Variation in human activity rates was explained by week day depending on daytime period (Table 2) but not by winter or month (Table 2). Disturbance events were much more frequent during weekend mornings (Table 2; Fig. 1a). Hunting activities occurred only during weekends and were more frequent during mornings (Table 2; Fig. 1b) but did not differ significantly between winters or months (Table 2). Farming activity rates were higher after weekends (Table 2; Fig. 1c) but did not differ between winters, months or daytime periods (Table 2). Finally, leisure activity rates varied significantly by winter, month and week day depending on daytime period (marginally significant; Table 2). Leisure activities were more frequent during weekend mornings (Fig. 1d), in winter 2011/ 2012 than in winter 2010/2011, and decreased throughout the winter (Table 2). Temporal variations in pin-tailed sandgrouse behaviour Pin-tailed sandgrouse in mixed flocks The proportion of pin-tailed sandgrouse in mixed flocks did not differ between winters or months but differed between week days depending on daytime period (Table 3). A greater
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Temporal variation in human disturbance rates
Response variable
Explanatory variables
χ2
Level estimates* df
P
Total human activity rate
Estimate ± SE
z value
P
Intercept (a)
0.94 ± 0.20
4.65
