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The distribution of animal populations across time and space varies according to a series of ecological variables in a given environment (Bell et al. 1994, Baudains and Lloyd 2007). Habitat selection is a behavioral response in animals, either innate or learned, which allows them to recognize and distin- guish various environmental elements, resulting in a differential use of the available resources (Block and Brennan 1993). This selection is observed through the distribution of species across the various types of environments in which they live, as a result of macro-environmental factors, which encompass the entire environment (Manly et al. 2002). Habitat selec tion also depends on micro-environmental factors, such as the selection of specific characteristics that benefit both the species and the individual, like tem peratura, vegetation height, type of vegetation, water and food availability (Hutto 1985, Block and Brennan 1993, Manly et al. 2002). The decision on where to nest and/or forage, given the variety of available are- as, can be complex and significant for the survival of a bird species, since this choice directly affects the individuals’ reproductive fitness and survival (Doligez and Boulinier 2008).
The Southern Lapwing Vanellus chilensis is a medi- um-sized bird (255-277g in weight, and 35-37cm full length), whose distribution spans from central-south- ern Ecuador and central-eastern Brazil to southern Argentina (del Hoyo et al. 1992, Santos 2010). This is a species that inhabits a large variety of environ- ments, commonly occurring in both dry and wet nat ural grasslands, coastal regions (Santos 2010), an- thropized grasslands (Moretti and Evangelista 2008, Kamp et al. 2015) and urbanized areas (Costa 2002). The Southern Lapwing displays a wide array of so cial and agonistic behaviors (Costa 2002, Delfino and Carlos 2020) related to intraspecific and interspecific interactions, including human beings, resulting from the species’ territorial and aggressive characteristics (Delfino and Carlos 2020).
Despite the Southern Lapwing’s broad geographic distribution across South American grasslands, the open plant formations in South America feature quite heterogeneous characteristics (Pillar et al. 2009) with regional specificities. These range from microclimat- ic components, such as relative humidity and tem- perature (Pillar et al. 2009), the presence of certain animal species and distinct plant formations, to vary- ing degrees of anthropic impact and human usage of these ecosystems (Sell and Figueiró 2011). The differ- ence between these environments implies that there may be some selectivity in the criteria employed by the species, favoring certain formations over others during feeding and breeding (Krebs and Davies 1997).
Given the intrinsic relationship between individ- uals and their environment, it is necessary to identi- fy the preferred habitats of a species to comprehend its ecology (Lorenz 1995), and the complex interac- tion between behavior and territoriality (Fretwell and Lucas 1969, Murray 1971). This is particularly important in species where aggressive interactions are prominent in their behavioral repertoire, as is the case for the Southern Lapwing (Delfino and Car los 2020). Studies on the Southern Lapwing in this sense also support the creation of animal manage- ment plans that minimize conflicts in places where this species and human beings overlap, as in parks, squares and football fields (Shwartz et al. 2008, Kamp et al. 2015). Furthermore, this information could help elucidate which factors influence the presence of these birds in certain natural environments, and how changes to it could affect their populations (Krebs and Davies 1997), assisting in the elaboration of manage- ment plans for these environments.
Therefore, the goal of this work is to investigate the habitat selection process of the Southern Lapwing within an urbanized area of southern Brazil’s Rio Grande do Sul state, verifying (i) its preference for cer- tain phytophysiognomies, or types of environment, at the macro-habitat scale; (ii) which environmental factors affect the decision of feeding and nesting ter- ritories, at the microhabitat scale; (iii) and verifying if there is a change in environmental selection between the species’ breeding and non-breeding seasons.
methods
Study Area
The study was performed in an area of approx- imately 40 hectares in the municipality of Torres (29°20’07”S, 49043’37”W), Rio Grande do Sul, dur ing the months of April and July 2018. The region’s climate is typically humid subtropical (Peel et al. 2007), with an average temperature of 19.3° C, and an annual relative humidity of 83% (Wrege et al. 2011). The area is located in the countryside, next to the Itapeva State Park, and features a considera ble heterogeneity of environments, such as forest, impacted and clean grasslands, fields with bushes, flooded areas, and anthropized areas, the latter rep- resented by roads and a few houses. The area is used for foraging and nesting by a population of Southern Lapwing (Delfino and Carlos 2020). Part of the area is employed as a place for sheltering and raising do- mestic animals, and for extensive animal husbandry, in addition to presenting a certain degree of anthropi- zation due to previous usage of the area as a disposal area for construction material and waste. Coexisting with the Southern Lapwings, there are farm animals like horses and cattle (HCD, personal observation).
Fieldwork
Habitat selection was evaluated in two catego- ries. The first category at a macro-habitat scale pre- sented six different vegetation physiognomies with- in the study area’s landscape. Sampling was carried out through visual observation of the individuals in the study area and produced presence/absence data. The observations were performed in April 2018 (non-breeding season) and in July 2018 (breeding season). Six kinds of environments were evaluated (Pillar et al. 2009) (Fig. 1), namely:
Clean Grassland: characterized by non-woody, herbaceous ground plants and by the absence of bushy formations. Native pastures prevail and the soil is almost entirely covered by vegetation.
Impacted Grassland: also characterized by a predominance of non-woody, herbaceous plants, such as various grasses. Here, there is human impact, such as construction materials and waste, in addition to greater soil exposure, which is sandier, constantly suffering from erosion.
Bushy Field: there is a growth in bushy vegeta- tion in this habitat, with prevalence of juvenile trees and small bushes. There are also large grass clumps, which makes the vegetation higher than in other hab- itats.
Flooded Areas: consists of clean or impacted grasslands in which there is a prevalence of humid or flooded zones throughout almost the entire year. These regions may occasionally run dry, in places with prolonged droughts, but generally remain sup- plied with water due to southern Brazil’s typical rain cycles.
Forest Areas: areas with higher and denser vegetation, featuring a more developed higher and intermediate layer, formed by woody, medium-sized species. Despite it being preserved for the most part, there may be human impact.
Rural Areas under Urban Pressure: comprises areas where there is almost no vegetation, with ex- posed soil and/or with human infrastructure on the terrain, like houses, yards, and roads.
The percentage estimation for each of the habi tat types was done based on on-site observation and analysis of satellite and aerial images from software such as Google Earth ®.
The second category at a micro-habitat scale took on-site environmental variables into consider- ation, where breeding or non-breeding individuals were observed. As in the previous category, these variables were gathered in April 2018, during the species’ non-breeding season, and in July 2018, dur- ing its breeding season. The identification of the life cycle stage of the individuals follows the behavioral descriptions of Delfino and Carlos (2020). Environ mental characteristics that potentially influenced the occurrence of Southern Lapwings were logged at each point: soil cover, vegetation height, edaphic ar- thropod diversity, number of farm animals (e.g., cattle and horses) and degree of anthropization in the area. To obtain data at the micro-habitat scale, 60 points were sampled throughout the area, with 100 m be- tween each point, and with caution to avoid overlap in data collection and assure sampling independence (Fig. 1).
Vegetation height and soil arthropod richness and diversity were estimated with the aid of a 30 x 30 cm board. Vegetation height was measured on the four sides of the board for subsequent averaging (Freitas and Magalhaes 2012), while edaphic arthropod rich- ness and diversity was accounted through the col- lection of a portion of the soil’s surface and tallying the total number of organisms and orders found for 5 minutes at each point (Copatti and Daudt 2009).
Soil cover was determined on a scale from 0 to 100, where the first value corresponds to fully exposed soils, and the last is fully covered by vegeta- tion (Brower et al. 1997, Santos and Nucci 2019). The extent of anthropization was applied in a subjective manner by the observer, on a scale from 1 to 3, being: (1) native terrain; (2) partially affected land; and (3) lands highly altered by human activity, completely modified relative to the original vegetation. This scale takes three aspects into consideration: natural ele- ments (e.g., fauna and flora), artificial elements (e.g., waste and pollutants) and human usage of the area (adapted from de Lima et al. 2004). The quantity of farm animals at each point was tallied through direct- ly counting the number of cattle and horses in a radi- us of 50 meters from each point. Other types of farm animals do not occur in the area. Data collection was made by the same observer and followed procedures and protocols described in the literature to avoid bi- ased evaluations (de Lima et al. 2004).
The occurrence of Southern Lapwing across the 60 points was assessed by direct observation of the birds by the same observer during five minutes per sampling point on five occasions in the month of April 2018 (non-breeding) and on another five occasions in July 2018 (breeding season), noting the presence or absence of the individuals through visual identifi cation in a radius of up to 50 meters from the center of the point (Sutherland et al. 2004). All the observa- tions were made during stable climatic conditions, without rain and strong winds, and during the after- noon. Flying birds were not counted (Sutherland et al. 2004).
Data analysis
To analyze macro-habitat selection, usage and availability of each environment type was examined (Neu et al. 1974), comparing the number of present individuáis in each environment to the number of ex- pected individuáis, by applying the chi-squared test (Krebs 1999). This data was also submitted to the In dex Selection calculation (Manly et al. 2002), to verify which macro-habitat was selected or rejected by the birds, considering a tolerance range based on the da- taset’s standard error.
For analysis at the micro-habitat scale, during both non-breeding and breeding seasons, multi- collinearity was verified by using Spearman’s rank correlation and variance inflation factor (VIF) tests (Zuur et al. 2010). We sequentially removed highly significant correlated covariates, as well as covariates with the largest VIF (> 5). Subsequently, a generalized linear model (GLM) analysis was performed to verify the species’ likelihood of presence at a given point, according to the study’s variables. The models were made with the presence and absence data (Loeys et al. 2012) and were analyzed using the function occu from the UNMARKED package (Fiske and Chandler 2011).
The selection of models was done using the step- wise regression method, employing the Akaike Infor- mation Criterion (AIC), arranging them based on the criterion’s weight (Burnham and Anderson 2002). A chi-squared test was performed to compare the var iables’ weights between non-breeding and breeding seasons (Krebs 1999). All data was normalized inde- pendently for each variable (Zar 2010) and all analy- ses were carried out in R software (R Core Team 2015).
results
Macro-habitat Selection
The study area was mainly composed of impact- ed grassland (29.4%), bushy (24.5%) and clean (22%) grasslands. The flooded areas contributed to 9.4%, forests to 8.4% and human areas to 6.2% of the total study area. With the goal of standardizing the study, changes in these proportions were disregarded be- tween the two observed occasions (April and July), since there were no meaningful differences (x2 = 30, df = 5, P = 0.2243).
We recorded 70 observations of Southern Lap- wing individuals during the non-breeding season and 44 during the breeding season. Macro-habitat analysis indicated that the birds do not haphazardly distribute themselves across the six habitats, but ac- tively select certain environments of the landscape, during both the breeding season X = 43.96, df = 5, P < 0.05) as well as the non-breeding season X = 58.27, df = 5, P < 0.05).
The calculation of the selectivity index (Table 1) suggested that there is a positive selection related to human areas and impacted grasslands, whereas forested areas and “bushy” fields featured a negative selection, suggesting that individuals avoid these for- mations. In the case of “clean” grasslands and flooded areas, there was a neutral selection, which suggests that birds occupy these regions on occasion. Between non-breeding and breeding seasons, there was a fluc- tuation in habitat selection only for flooded areas: while during the non-reproductive season the selec- tion was neutral, during the reproductive season it was avoided by the lapwings.
Micro-habitat Selection
Regarding micro-habitat selection, the correlation analyses indicated that there was a direct correlation between arthropod diversity and the other variables, a tendency that was confirmed by calculating the VIF, which surpassed the limit considered acceptable for the work (i.e., VIF = 5). This variable was therefore excluded from subsequent analyses. Fifteen models were obtained with the remaining variables, includ- ing all combination possibilities between them for non-breeding and breeding seasons, totaling thirty models analyzed (Table 2).
The generation of models and gradual stepwise selection through AIC indicated that the best mod- el to explain the components that affect the occur- rence of Southern Lapwing in the study area during the non-breeding season (AIC = 189.13, AICw = 0.5) is the one that includes vegetation height (K = -2.84, P < 0.05), the presence of farm animals (cattle and horses) in the area (Z = 2, P = 0.03) and the degree of human impact (Z = 1.82, P = 0.04) (Table 3). The first component was negatively related to the presence of the species, suggesting that there is a selection for en- vironments with low vegetation, in addition to a pos- itive correlation with more disturbed environments and environments with farm animals, showing a certain preference for these types of habitats.
Brazil. The white points indicate the sampling points of micro-habitat variables, distributed over the study area.
Table 1: Selection index (W) calculated from use and availability data of each environmental category, according to Neu et al. (1974) and Manly et al. (2002). Values below 0.85 indicate negative selection, values above 1.15 indicate positive selection, and values between 0.85 and 1.15 indicate neutral selection.
Table 2: All the models that were taken into consideration in the micro-habitat selection analysis. The models were constructed combining all four environmental variables remaining after correlation analyses and applied both in the non-breeding and the breeding season (hveg = vegetation height; numdom = number of farm animals; imphum= degree of anthropization; gcov= soil cover).
Table 3: Best three Generalized Linear Models (GLM) during both non-breeding and breeding seasons, with AIC score, delta AIC and the cumulative weight of each model, respectively (hveg = vegetation height; numdom = number of farm animals; imphum = degree of anthropization; gcov= soil cover).
During the breeding season, the most suitable model (AIC = 187.92, AlCw = 0.34) included vegetation height (Z = - 2.34, P = 0.02) and presence of farm
animals in the area (Z = -1.76, P = 0.08) (Table 3). The species presented an affinity for low-vegetation en- vironments during breeding but avoided places with the highest presence of large-sized farm animals dur- ing this period.
The comparison between breeding and non-breeding seasons revealed that, concerning the human impact and presence of farm animals, there was a considerable difference between seasons (t = 8.82, df = 90.34, P < 0.05). However, the variable vegetation height, which tends to be one of the most selected in the models across both seasons, did not significantly differ between the sampled periods (t = 0.60, df = 114.34, P = 0.55).
discussion
In spite of Southern Lapwing being described as a species "typical of low altitude grasslands [...] where undergrowth prevails, but also tolerating degrad- ed habitats and human presence” (Santos 2010), no study had been performed to gauge the bird’s habitat selection. Analysis at the macro-habitat scale con- firms that the species possesses a strong affinity for impacted grasslands and urban area environments, which was strengthened by micro-habitat analy- ses showing that factors such as human impact and presence of farm animals, in addition to vegetation height, are part of this species’ selection process. This demonstrates that there is a relationship be- tween the occurrence of this species and human ac- tivity, even if the causes of this relationship are not yet fully understood.
Many species of animals are considered synan- thropic, benefitting from environments occupied by human beings (Marzluff et al. 2001). These benefits may arise due to three interrelated reasons: (1) great- er resource availability provided by the large volume of organic waste which can be used for feeding (Faeth et al. 2005); (2) protection against predators (Rode- wald et al. 2011), since there is a tendency towards lesser predation pressure in urbanized environments (Sorace 2002), and (3) diminished interspecific com- petition, as fewer species occupy these environments (Shochat et al. 2010). Indirect beneficial relationships can also emerge, where some species flock to urban environments due to the presence of domestic or farm animals (Rodewald 2012).
Human occupation and habitation have creat- ed a new ecological niche in natural environments, which seems to be little exploited by some bird species (Rodewald 2012, Santos and Cademartori 2015), but may be advantageous for generalist species with preferences for low vegetation, such as the Southern Lapwing. With the opportunity to occupy these new territories, there may be benefits regarding greater access to food resources and protection from preda- tory birds (Faeth et al. 2005). This could be a result not only of habitation of areas where human construc- tion occurs, including the presence of buildings and roads, but also by occupying grasslands where farm animals are raised (Cardoni et al. 2015). In addition, the Southern Lapwing’s high capacity for surviving in environments under severe environmental pressure (Santos 2010), in contrast with other more sensitive birds (Stanton et al. 2018), and its territorial, typically aggressive behavior (Delfino and Carlos 2020), grantsTable 3. Best three Generalized Linear Models (GLM) during both non-breeding and breeding seasons, with AIC score, delta AIC and the cumulative weight of each model, respectively (hveg = vegetation height; numdom = number of farm animals; imphum = degree of anthropization; gcov= soil cover).
Season Models AIC deltaAIC Cumulative wt.
hveg + numdom + imphum 189.14 0.00 0.5
Non-breeding sea- hveg + nundom
son
hveg + gcov + numdom + imphum hveg + numdom
Breeding season hveg + numdom + imphum
Hveg them greater reproductive and survival success in these environments (Saracura 2003).
In rural areas, the main human impacts on natu ral vegetation are caused by agriculture and animal husbandry (Albaladejo 2006, Wagner et al. 2013). In animal husbandry, large and medium sized animals are frequently raised in an extensive manner across native grasslands, a historically widespread practice in southern Brazil (Crawshaw et al. 2007). These ani mals, bovines and equines for the most part, use the area for foraging and as a consequence drastically alter the landscape of the native grasslands (Brown and McDonald 1995). The major observed change is the considerable reduction in vegetation height when compared to places where there is no grazing activity, nor farmed animals (Adler and Hall 2005). Thus, the usage of native grassland areas for extensive animal husbandry results in grasslands with lower vegeta tion height and less arboreal and shrub species (Hen- dricks et al. 2005). Furthermore, the presence of cat- tle directly modifies the physicochemical atributes of the soil (Rodríguez-Medina and Moreno-Casasola 2013, Carvalho et al. 2018), which benefits part of the area’s edaphic fauna, primarily certain groups of invertebrates, such as Coleoptera, Hymenoptera (For- micidae), and Diptera (Cunha Neto et al. 2012, Hoff- man et al. 2018), that comprise the main food source of the Southern Lapwing (Santos 2010).
The presence of farm animals directly influences two of the main characteristics selected by Southern Lapwing: vegetation height and soil arthropod rich- ness. This explains the bird’s high affinity for environ ments with husbandry activity and could also explain its expansion towards northern Brazil (Santos 2010).
The progress of deforestation and husbandry activi- ties in the region (Rivero et al. 2009, Domingues and Bermann 2012) ends up creating territories where Southern Lapwings can forage and establish breeding populations. Additionally, behavioral studies suggest that a positive relationship between Southern Lap- wings and cattle or horses may be established during the non-breeding season (Delfino and Carlos 2020). However, during the breeding season the tendency is reversed and the presence of large animals within the nesting grounds becomes detrimental, seeing as there is a risk of trampling of their eggs and chicks (Mandema et al. 2013, Sabatier et al. 2015).
The rejection of environments with higher arbo- real layers, such as bushy fields and forests, supports the hypothesis of preference by Southern Lapwings for open formations, which goes back not only to the species’ behavioral aspects, but also aspects shared by its congeners: most of the species in the Vanellus genus are species of grassland environments and typically low-vegetation areas (Bolton et al. 2007, Düttmann et al. 2018, Mishra et al. 2018, Cantlay et al. 2019). In such environments, these birds can more easily watch and protect their nests (Saracura 2003).
The primary predators of Southern Lapwing adults and chicks are birds of prey like the Southern Caracara (Caracaraplancus), Chimango Caracara (Mil- vago chimango), Savanna Hawk (Heterospizias meridion- alis), Long-winged Harrier (Circus buffoni), Burrowing Owl (Athene cunicularia), as well as the Black Vulture (Coragyps atratus) (Belton 1994, Costa 2002, Santos 2010), which often employ aerial attacks. Thus, in- habiting open environments with low vegetation al- lows the Southern Lapwing to have more space for ob- servation and more time for defensive reaction, such as escape or successful agonistic response against the attacker (Delfino and Carlos 2020).
The use of clean and flooded grasslands was neu tral during the observed period, especially during the non-breeding season, when these environments were occasionally utilized for foraging (HCD, personal ob- servation). However, the negative selection of flooded field environments during breeding season can be explained by the dynamics and architecture of nest building. Southern Lapwings place their eggs directly on the soil (Saracura 2003), in simple and open nests with few deposited materials (Simon and Pacheco 2005). As such, flooded environments pose a poten- tial risk for the nests’ reproductive success, and are consequently avoided during that time of the year.
The study also demonstrated that, despite vegeta- tion height being the most impactful for habitat and territory selection, there is a plasticity that varies with the species’ breeding cycle, as the environment’s se- lected characteristics begin to change between breed- ing and non-breeding seasons. Ultimately, this work elucidates the intrinsic relationship between human beings, the rural environment and the Southern Lap- wing, relating environmental factors to the species’ behavioral aspects and the ecological dynamics of these environments. It also supports the elaboration of hypotheses on why the species has been striking- ly expanding its area of distribution in tandem with the Brazilian agricultural frontier and why, unlike its Old World congeners (Galbraith 1988, Baines 1990, Peach et al. 1994), this species tends to have its life cycle increasingly intertwined with human activities, be it in rural or urban areas.
acknowledgments
We thank Torres city hall for allowing the comple- tion of this research within city limits and the LAB- SMAR/UFRGS for the support and infrastructure for the development of this paper. We also thank the two anonymous reviewers that helped to improve this manuscript through their valuable commentary and observations. HCD and CJC respectively received a master’s and a postdoctoral fellowship from the Coordenapao de Aperfeipoamento de Pessoal de Nivel Superior (CAPES), Brazil.
