Winter Ecology of Agricultural Birds: The Role of Crop Type in Habitat Occupation by the Eurasian Blackcap

Abstract

Agriculture is an anthropic activity with a significant impact on the environment and biodiversity. Hence, the conservation and proper management of wildlife inhabiting agricultural areas is crucial to ensure both food production sustainability and biodiversity preservation. The presence and distribution of the Eurasian Blackcap (Sylvia atricapilla) was evaluated in different crops during winter and the influence of vegetation structure and altitude on its abundance was analyzed. It was hypothesized that the presence and abundance of the species would be influenced by vegetation structure and altitude. Sampling was conducted in 60 agricultural plots differentiating homogeneous and heterogeneous crops. Warblers were recorded by sight and hearing along 1 km transects. The effect of vegetation structure on the warbler abundance was analyzed by carrying out ANOVAs and Mann–Whitney tests. The Eurasian Blackcap was detected in 75% of the sampled plots. Significant differences in vegetation structure between occupied and unoccupied crops were not found; however, an effect of the altitude of the transects was observed, occupying mostly lower areas. The warbler abundance was not significantly affected by crop type nor sampling year. This study provides valuable information on the ecology and distribution of the Eurasian Blackcap in agricultural crops, enriching the knowledge on how to establish the sustainable management of croplands and ensure the conservation and proper management of the species in agricultural areas.

1. Introduction

Winter represents a critical period for birds, as it is especially challenging to find the most favorable conditions and ensure their survival. According to Jokimäki et al. [1], in winter, birds tend to prefer lower altitudes due to an increased thermal expenditure. Lower altitude zones also provide greater primary production, favored by higher temperatures and more accumulated precipitation, facilitating the settlement of migratory birds [2,3,4].

In the Iberian Peninsula, during winter, the areas with the richest bird populations are mainly found in the north-east, the Ebro Delta, and the large coastal wetlands, especially on the Mediterranean coast [4,5]. The latter is the main wintering site for most presaharian migratory passerines [6], favoring the diversity and population size of species in Mediterranean ecosystems [7,8].

Studies on bird wintering site selection have been focused on altitudes higher than 1000 m and used different spatial approaches, including ecological units such as vegetation structure, food availability, geographical location, and climate to explain species selection [3,9,10,11,12,13,14]. However, there is a lack of studies that examine the occupation of species that select ecosystems at lower altitudes, and even fewer that consider the role played by transformed ecosystems such as crops [2,7,15,16,17,18].

Several studies showed that different elements of the landscape have a complementary effect on bird fauna throughout the annual cycle. In particular, during the seasonal movements that species make during winter, a marked preference for agricultural areas has been observed [18,19,20,21,22,23]. In these areas, in addition to crop coverage, rainfall abundance plays a decisive role in increasing productivity, which, in turn, results in a suitable wintering habitat for birds exploiting the temporary abundance of plant-based resources [4].

Birds selecting crops have developed adaptations to take advantage of the temporary abundance of plant resources in cultivated areas [24]. In general, spatial heterogeneity does not seem to be very important in the abundance of birds in agricultural systems, regardless of the type of crop [25,26]. However, some studies indicate that habitat heterogeneity can be an important factor determining bird occupation [17,18,27,28,29,30] and diversification [31].

The Eurasian Blackcap (Sylvia atricapilla L. 1753) is a migratory warbler species from Central Europe that traditionally winters in coastal Mediterranean areas [32,33]. This species is a frugivore known to have an important effect on seed dispersal of several plant species (e.g., Pistacia lentiscus [34]), where it has been observed to have a strong relationship with anthropized areas, especially agricultural regions [22,35,36,37,38]. In Spain, its presence has been recorded in a wide variety of crops, including onion, tiger nut, potato, watermelon, oranges, vines, cereals, and olives [15,18,20,28,39]. This preference for cultivated areas during winter migration over natural forest areas makes this species an interesting study object. However, most studies focus on olive plantations, where the presence of warblers has been interpreted as a pre-adaptation to these crops [15].

Fruit availability has been identified as one of the best predictors of the abundance of wintering Eurasian Blackcaps in Mediterranean environments [9,40,41,42]. Some authors even observed that this species tracks the availability of olives at local and regional levels [40,43], suggesting that individuals have similar access to food resources across all sites [40].

The winter season has a significant impact on bird dynamics and determines their migratory movements to optimal sites. In this study, we investigated the winter occupation of crops by the Eurasian Blackcap (Sylvia atricapilla). Our specific objectives included identifying the variables that influence the species’ habitat occupation and, in this regard, revealing the crucial role played by the crop’s vegetation structure in the distribution and abundance of the Eurasian Blackcap, as well as discovering possible variations in its occupation among different types of crops. In this sense, our hypothesis posits that the presence and abundance of the Eurasian Blackcap in orange crops are closely related to the vegetation density and altitude of the study area. Additionally, we anticipate that certain types of crops may be more conducive to attracting this migratory species, which could be reflected in significant differences in the species’ occupation among the different crops.

2. Material and Methods

2.1. Study Area

The study site was located in eastern Spain, in the Province of Valencia (39°20′00″ North, 0°50′00″ West) (Figure 1). The area is dominated by a Mediterranean climate. Thus, the natural vegetation in the province is typical Mediterranean, including holm oak (Quercus ilex L. 1753), gall oak (Quercus faginea Lam. 1785), cork oak (Quercus suber L. 1753), Pine (Pinus sp.), rosemary (Rosmarinus officinalis L. 1753), thyme (Thymus vulgaris L. 1753), and juniper (Juniperus phoenicea L. 1753), among others. Shrub species recorded include mastic tree (Pistacia lentiscus), reed (Phragmites australis (Cav.) Trin. ex Steud. 1841), and kermes oak (Quercus coccifera L. 1753). Herbaceous species include cat’s claw (Uncaria tomentosa Willd. ex Schult. DC. 1830), asparagus (Asparagus acutifolius L. 1753), and poppy (Papaver pinnatifidum Moris 1837), among many others. However, due to human activity, these natural habitats have been altered and now coexist with large areas of crops, mainly orange (Citrus sinensis (L.) Osbeck 1765), mandarin (Citrus reticulata Blanco 1837), lemon (Citrus limon (L.) Burm. Fil. 1768), olive (Olea europaea L. 1753), peach (Prunus persica (L.) Stokes 1812), pomegranate (Punica granatum L. 1753), persimmon (Diospyros kaki L.f. 1782), Carob (Ceratonia siliqua L. 1753), loquat (Eriobotrya japonica Lindl. 1821), cherry (Prunus avium L. 1755), almond (Prunus dulcis (Mill.) D. A. Webb 1967), walnut (Juglans regia L. 1753), and vine (Vitis sp.).

2.2. Bird Sampling

During the winters (December–February) of 2015 and 2016, we censused Eurasian Blackcaps (Sylvia atricapilla) in a total of 60 locations in the Province of Valencia. The methodology used was similar to the method used in another study by the same authors [44]. For this purpose, we established one-kilometer linear transects [45] whose distance was measured using a GPS (eTrex). In each transect, we recorded all individuals sighted or heard. Each location was visited once during each winter season, and the censuses were conducted by the same researcher (EAAM) at a sampling speed between 15 and 20 min to avoid the repeated counting of individuals. The censuses were carried out 30 min after sunrise, and the starting time varied as the winter season progressed. No censuses were conducted during adverse weather conditions, such as heavy rain or excessive wind.

The intersection point method was applied to record the vegetation present in each transect [46]. This method allowed to record the composition of the vegetation, determining the coverage of each species at different strata [46,47,48]. At each location, we traced five 25 m transects perpendicular to the listening transect and recorded every plant species with a height greater than 0.3 m that touched the line. The documented variables included plant coverage (%), plant height (m), and species richness. The length of the transects was measured with a rope, and the geographic position and height above sea level (altitude) of each transect were recorded using a GPS.

Using the vegetation data gathered, it was possible to distinguish two types of crops: homogeneous and heterogeneous. Homogeneous crops were defined as extensive areas dominated by a singular crop species, like olives (Olea europaea L., 1753), mandarins (Citrus reticulata Blanco, 1837), oranges (Citrus sinensis L., 1753), carob trees (Ceratonia siliqua L., 1753), and almonds (Prunus dulcis (Mill.) DA Webb). Heterogeneous crops, on the other hand, were characterized by the coexistence of three or more vegetal species, forming diversified agricultural systems. In addition to the above mentioned crop species (among others), adjacent arboreal species could also be observed, like pines (Pinus sp.) and walnuts (Juglans regia L., 1753); also bush species like Pistacia lentiscus (L., 1753), Phragmites australis (Cav. Trin. Ex Steud., 1841), and Quercus coccifera (L., 1753); and, finally, herbaceous species like Uncaria tomentosa (Willd. Ex Schult., DC., 1830), Rosmarinus officinalis (L., 1753), Asparragus acutifolius (L., 1753), Papaver pinnatifidum (Moris, 1837), and many representatives of the Asteraceae family. Considering the distance of the transects (1 km), an approximated hearing distance of 200 m in each direction of the transect (pers. obs.), and the number of transects in each type of crop (23 homogeneous and 37 heterogeneous), the sampling area included 920 Ha (32%) of homogeneous crops and 1480 Ha (61%) of heterogeneous crops. This relation reflects the distribution of both types of crops in the general study area (pers. obs.).

2.3. Data Analysis

In order to assess landscape complexity we used richness, evenness, and dominance indices calculated using the Past version 3.17 program [49], taking into account the number of elements, interactions, and connectivity according to Papadimitriou’s (2002) [50] landscape function. Then, we carried out a Shapiro–Wilk normality test of the following variables: altitude, height, vegetation cover, richness, evenness, and vegetation dominance. The differences in those variables between occupied and unoccupied crops, as well as between years, were analyzed by t-tests in the case of normally distributed data and non-parametric Mann–Whitney U tests for non-normally distributed data. To analyze differences in the abundance of the Eurasian Blackcap between types of cultivation and sampling years, a two-way ANOVA was used, followed by a linear regression analysis to determine the relationship between species abundance and the structural characteristics of homogeneous and heterogeneous crops. The XLSTAT-Ecology version 5 (2017) [51] statistical program was used to perform the tests.

3. Results

A total of 215 individuals of the Eurasian Blackcap were detected during the study, in 75% (N = 45) of the sampling points. Although no significant differences were found in the vegetation structure between the crops occupied and not occupied by the species, variations were observed based on altitude (

Table 1. Mean ± standard deviation of the studied variables, together with the results of the statistical tests (t-test for normally distributed variables and Mann–Whitney U test for non-normally distributed variables) comparing occupied and non-occupied crops.

Variables	Occupied (N = 45)	Non-Occupied (N = 15)	t	df	p
Coverage	42.8 ± 24.5	37.9 ± 19.3	−0.71	58	0.48
Richness	0.98 ± 0.01	1.01 ± 0.04	0.19	57	0.85
Dominance	0.48 ± 0.00	0.47 ± 0.01	0.13	57	0.89
Evenness	0.85 ± 0.00	0.91 ± 0.01	0.7	54	0.48
			U		p
Height	2.28 ± 0.87	1.93 ± 0.79	265		0.22
Altitude	181 ± 3.86	438 ± 19.9	499.5		0.001

). In particular, the crops where the species was present were located in altitudes significantly lower (181 ± 3.86 masl) than those of non-occupied areas (438 ± 19.9 masl).

The results of the two-way ANOVA analysis did not indicate significant differences in the abundance of the species with respect to the type of crop and sampling year (F2, 44 = 1.81; p > 0.05; Figure 2). However, a general tendency towards higher abundances in heterogeneous crops (N = 143) compared to homogeneous crops (N = 73) could be observed. Also, the number of individuals observed was higher in 2014 (n = 153) than in 2015 (n = 62).

Although no significant differences were found in vegetation richness between homogeneous and heterogeneous crops (Mann–Whitney U: U = 125.5; p > 0.05), differences in dominance and evenness were observed. In particular, it was found that homogeneous crops showed a higher mean dominance value (0.52 ± 0.13) compared to heterogeneous crops (0.43 ± 0.12) (Mann–Whitney U: U = 87.5; p < 0.05), while evenness reached its maximum value in the heterogeneous crop (0.83 ± 0.03) (

Table 2. Mean ± standard deviation of vegetation indices for each crop and results of the statistical tests (t-test) comparing homogeneous and heterogeneous crops.

	Homogeneous	Heterogeneous	t	df	p
Margalef	0.74 ± 0.03	1.11 ± 0.02	1.74	43	0.09
Evenness	0.57 ± 0.02	1.04 ± 0.01	3.24	43	<0.01
Dominance	0.67 ± 0.01	0.42 ± 0.00	−4.51	43	<0.01

).

According to the regression analysis, none of the structural characteristics of the habitat showed a significant relationship with the abundance of the species in the crops (Figure 3), and similar trends were observed in both types of crops.

4. Discussion

According to our results, the Eurasian Blackcap selects different types of crops as its winter habitat and the species abundance does not appear to be related to the structural organization of the crop. These findings support the results of other studies suggesting the species’ preference for anthropogenic crop habitats for wintering [9,15,18,22,28,30,33,43,52]. Apparently, the intensification of cultivation does not necessarily reduce its suitability as a winter habitat for frugivorous birds [30]. Although we did not find differences between habitat characteristics of occupied and unoccupied crops by the species, the clear variation in the altitude at which habitats were located could explain the changes in spatial occupation recorded in crops. It has been shown that the altitudinal effect on the distribution of migratory birds occurs at high altitudes [11,12], reflecting plasticity in the species’ selective behavior in response to the current climate [14,41]. Our study suggests that this pattern can also occur at low altitudes, where species may find greater food availability and milder temperatures. Other studies have observed that spatial variation in climate explains variation in bird occurrence, generating limitations in their distribution within their preferred habitats during winter; in fact, it has been found that during winter, species track the availability of their preferred habitats within their climatic limits over time [53].

In addition to the structural organization of the crop, it is important to consider other habitat variables such as height, coverage, and richness in the habitat selection of birds [2]. Although in our study these variables did not show statistical differences, it is possible that in other contexts they may be related. In fact, it has been shown that sylvids are more attracted to densely foliated trees, which is considered a response to reduce the probability of predation during feeding [54]. On the other hand, bird abundance seems to decrease with increasing crop complexity [30,55], and in our study, we found that crops with greater vegetation richness were not occupied by the species. It is important to note that these results may be influenced by food availability, as greater vegetation richness does not necessarily imply greater food availability for birds [55]. In fact, in a recent study in Britain and Ireland [56], the authors found that changes in food availability (in this case, backyard bird feeding) modifies S. atricapilla winter ecology. Another factor to take into account is that migrating birds, like warblers, seem to choose stopover sites also on acoustic clues, specifically the presence of singing conspecifics, as shown in a recent study [57].

The results of our study indicate that small-scale crop complexity, in terms of homogeneity and heterogeneity, does not appear to be an important variable in explaining the abundance of the Eurasian Blackcap in Mediterranean perennial agricultural systems. Consistently with Castro-Caro et al. [25] and Peréz et al. [30], we found no relationship between bird abundance and landscape structure. In winter, surplus fruit is a crucial resource that drives field selection by birds [31]. The species’ ability to track changes in patch-scale food availability [43] and its transient foraging strategy [4,52] appear to facilitate crop exploration regardless of its structure. Additionally, some populations of the Eurasian Blackcap have undergone evolutionary changes in migratory behavior as a result of environmental and habitat changes caused by human activities, which have preceded changes in the selection of winter habitat for this species [58]. This behavior may be aided by the dominance of the surrounding matrix and the size and distribution of the crop [28]. It has been observed that Eurasian Blackcap abundance responds even to crop use dynamics, with density decreasing after harvest [43]. Additionally, in perennial crops, the degree of disturbance generated by management is much lower than in other types of crops [59]. In these crops, the proportion of seasonal resources is more predictable for species and acts as alternative habitats for bird communities, particularly migratory species [15].

The available information on winter bird occupancy in orange crops is limited [18,20,39,52,60]. However, it is known that in southeastern Spain, these agricultural systems are a common winter habitat for the species, being a habitat chosen by the species even more than its natural habitat, regardless of the season [18]. In this type of habitat, it seems to feed on fallen oranges, which become a resource available throughout the winter. Additionally, the strategy of pecking at the pulp plays an important role in this bird species when the consumed fruit is difficult to manipulate and swallow whole [61,62]. This pre-adaptive characteristic of pecking at fruit allows frugivores to survive in farmlands where fruit size has been increased by artificial selection [15,62].

In the Eurasian Blackcap, this behavior has also been reported in olive plantations, where it appears to be particularly frequent and is interpreted as an opportunistic feeding behavior to cope with low fruit availability [15]. On the other hand, it is possible that, as with olives [15,30], oranges are a predictable winter resource for the species at the regional level and that the little intrinsic variation in their availability, phenology, and distribution promotes the occupancy of orange crops by the species throughout the season.

It has been suggested that the Eurasian Blackcap has pre-adaptations to ensure the use of cultivated habitats [58,60,61], and even the presence of resident populations of the species in this habitat has been observed [6,58,63,64,65]. This indicates the need to consider this information in the design of future cultivated habitat management strategies, as they could affect the population dynamics of the species inhabiting them. Although the species does not appear to be affected by the local structure of the crop, the intensification of agricultural practices, the type of landscape, and the harvest can affect food availability for birds [15], which could generate different behaviors in the movement of migratory populations within the crop [52].

In the specific case of orange crops, the winter habitat occupation by the Eurasian Blackcap could be favored by the reduction in recent years of the intensification of agricultural practices, which facilitates the colonization of the species. However, the increasing spatial heterogeneity of the orange crop could affect the connectivity between patches and alter the way in which populations of migratory birds occupy this type of habitat. Therefore, it is necessary to discover the threshold at which the spatial heterogeneity of the crop affects the change in the movement dynamics of migrating (sedentary or transient) populations, in order to propose management alternatives for the maintenance and conservation of this and other species in anthropic habitats such as crops.

In conclusion, our results provide important information on the distribution and abundance of the Eurasian Blackcap in different agricultural crops, as well as on the vegetation structure and its relationship with the species’ presence. Our results suggest that the presence of the Eurasian Blackcap could be influenced by factors other than the ones studied, such as food availability or the presence of suitable nesting habitats. They also highlight the importance of heterogeneous crops for maintaining biological diversity, as these crops had a higher species evenness compared to homogeneous crops. Overall, our research provides valuable information for the conservation of the Eurasian Blackcap and for the design of crop management strategies that promote biodiversity in agricultural systems.