The species and functional diversity of birds in almond orchards, apple ...

CSIRO PUBLISHING

Emu, 2015, 115, 99–109 http://dx.doi.org/10.1071/MU14022

The species and functional diversity of birds in almond orchards, apple orchards, vineyards and eucalypt woodlots Gary W. Luck A,C, Kelly Hunt A and Andrew Carter A,B A

Institute for Land, Water and Society, Charles Sturt University, PO Box 789, Albury, NSW 2640, Australia. Australian Wildlife Conservancy, Suite 5, 280 Hay Street, Subiaco, WA 6008, Australia. C Corresponding author. Email: [email protected] B

Abstract. Agriculture is the predominant land use in Australia. Yet, there is limited knowledge of which bird species use particular agricultural crops and the implications this has for crop damage or the provision of ecosystem services. We measured species and functional diversity of bird communities in almond and apple orchards, vineyards and eucalypt woodlots. Mean bird species richness was highest in almond orchards and eucalypt woodlots and lowest in vineyards. Species diversity was highest in almond orchards, but similar among the other land uses. Bird community composition clearly differed among land uses, indicating the need to treat particular crop types as different ‘habitats’. The functional diversity of bird communities differed across land uses dependent on the functional traits and metric used to calculate diversity. Eucalypt woodlots had the highest functional richness of bird reproductive traits, whereas the highest richness of bird foraging traits was recorded in almond orchards. Importantly, increasing land-use intensification did not reduce functional diversity in a consistent way. Bird species that may damage crops or help control crop pests were common across land uses. Moreover, we recorded large numbers of the threatened eastern subspecies of the Regent Parrot (Polytelis anthopeplus monarchoides) in almond orchards. Future management of Australian agro-ecosystems should find an appropriate balance between bird conservation, limiting costs from bird damage, and promoting the provision of ecosystem services by birds. Additional keywords: agriculture, crop damage, ecosystem services, farmland, functional traits, horticulture. Received 28 February 2014, accepted 15 December 2014, published online 10 April 2015

Introduction Over 40% of the Earth’s land surface is used for agriculture (MEA 2005). In Australia, ~60% of the continent is devoted to agricultural production (ABARES 2010). Global population growth means that the area of agricultural land or production intensity will have to increase to meet future food demands (UN DESA 2011). The spread of agriculture has had substantial negative impacts on native species, including a reduction in biological diversity and the local extinction of particular species (Best et al. 1995; Robinson and Sutherland 2002; Butler et al. 2007; Haslem and Bennett 2008a; Karp et al. 2012). This is especially true for birds, which have suffered major declines globally owing to agricultural development (Yahner 1982; Green et al. 1994; Thiollay 1995; Daily et al. 2001; Murphy 2003; Heikkinen et al. 2004; Azhar et al. 2011). In an attempt to develop more environmentally sustainable agricultural practices, some European countries have implemented agri-environmental schemes, but results for bird communities have been mixed (e.g. Kleijn et al. 2001; Peach et al. 2001; Baines et al. 2002; Kleijn and Sutherland 2003). Managing agro-ecosystems to reduce negative impacts on birds requires a better understanding of which species use particular agricultural land uses. Moreover, the types of birds using specific crops can Journal compilation
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have major implications for agricultural production primarily through two avenues. First, there is increasing interest in the ecosystem services (ecosystem functions that benefit humans) that birds can provide agriculture, which can reduce costs to growers and improve crop yield (Whelan et al. 2008). These include pollination of food crops, biological control of pests, disposal of waste and cycling of nutrients, to name a few (reviewed in Sekercioglu 2006; Whelan et al. 2008; Wenny et al. 2011; Triplett et al. 2012). Second, bird damage to certain crops (e.g. stone fruits, pome fruits, nut, berry and grain crops) can have major negative impacts on production (Avery 1984; Bomford and Sinclair 2002; Tracey et al. 2007). In agricultural landscapes, conservation–production interactions have complex implications whereby changing management strategies can support or discourage particular bird species either to the benefit or detriment of growers and bird conservation. Based on a systematic review of the literature, Hunt (2013) found that in community-level studies of birds in agricultural landscapes in Australia, 41% of 103 sites across 53 studies were focussed on patches of remnant native vegetation, regrowth or native plantings. While this focus gives some insight into the community profile of birds occurring in the broader landscape, it provides little information on which species use particular www.publish.csiro.au/journals/emu

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agricultural crops. In the studies reviewed by Hunt (2013), surveys within production lands focussed mostly on grazing land/pasture (23% of 103 sites), with few surveys occurring within horticultural crops (9%) or native timber plantations (5%). Hence, some crop types have been relatively undersampled in Australia, resulting in limited knowledge of the support agricultural lands may provide bird communities, or how bird community composition may influence production through crop damage or the provision of ecosystem services. The positive or negative impacts of birds in agricultural landscapes result from the activities they engage in, which in turn is related to their functional traits. A functional trait is defined as any morphological, physiological, phenological, or behavioural characteristic of an individual (Violle et al. 2007; Luck et al. 2012). For example, relevant traits for birds include body mass, bill length, clutch size, foraging behaviour and habitat use. Promoting a diversity of traits – ‘functional diversity’ – is crucial for the maintenance of a range of ecosystem functions. Yet, agricultural intensification can reduce functional diversity, resulting in an uncertain future for some ecosystem functions (Collard et al. 2009; Flynn et al. 2009). While measures of species diversity have historically dominated community-level bird studies, greater attention is now being focussed on changes in functional diversity (Sekercioglu 2006; Luck et al. 2013b). This builds on previous work focussing primarily on bird foraging guilds (e.g. Curry 1991; Loyn et al. 2007; Barrett et al. 2008). Here, we examine the species and functional diversity of bird communities occupying four different agricultural land uses in south-eastern Australia. Our aim is to document differences in these measures across land uses and identify species associated with particular land uses. The land uses we included were as follows: (1) eucalypt woodlots grown for firewood, (2) almond orchards, (3) apple orchards, and (4) vineyards. Given the results of past studies (e.g. Flynn et al. 2009), we hypothesised that bird species diversity and functional diversity would be highest in eucalypt woodlots owing to their similarity to surrounding native vegetation, and lowest in vineyards because these did not have a treed overstorey. However, functional diversity can be measured in different ways (see Methods) and different components of diversity may vary unexpectedly and inconsistently across land uses (Luck et al. 2013b). We were also interested in whether each land use supported a substantially different bird community, to test the assertion that different agricultural crops should be treated differently when considering their interactions with birds. Methods Study sites Birds were surveyed between November 2009 and October 2010. Surveys were conducted in six mature (i.e. trees planted during 1990–2000, and producing fruit) almond orchards that comprised an extensive plantation (15 646 ha) located immediately south of Robinvale, north-west Victoria (34
580 1200 S, 142
760 5700 E). The average size of almond blocks is ~17 ha and these blocks are embedded (occur side by side) in orchards [farms] ranging in size from 145 ha to 1717 ha. Regional climate is semiarid and the mean annual rainfall is 267 mm (BOM 2013a). Native vegetation in the study area is characterised by black box (Eucalyptus largiflorens) and mallee (e.g. E. gracilis and

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E. incrassata) woodlands, and river red gum (E. camaldulensis) forests along water courses. The landscape is dominated by various farming enterprises including dryland cereal crops and irrigated horticultural crops such as grapes, olives, almonds and citrus. Birds were surveyed in seven mature (i.e. trees planted during 1995–2001, and producing fruit) apple orchards around Shepparton (36
380 1500 S, 145
390 8100 E), in central northern Victoria, where the climate is temperate and the mean annual rainfall is 447 mm (BOM 2013b). Apple orchards ranged in size from ~20 ha to over 150 ha, and the total area of apple orchards around Shepparton is over 1900 ha. Remaining native vegetation is primarily grassy or floodplain woodland or forests along water courses, with common overstorey species including E. camaldulensis, E. macrocarpa, E. albens and E. largiflorens. The region has a long history of irrigated agriculture and today it is one of the largest irrigated areas in Australia with common crops including apples, pears, peaches and apricots (ABS 2006). Surveys of birds in five mature vineyards (all >10 years old) were conducted in both the Wangaratta (specifically near the Warby–Ovens National Park; 36
310 6200 S, 146
160 8800 E) and Rutherglen (36
050 2400 S, 146
460 9500 E) growing districts, north-east Victoria. Vineyard size ranged from ~100 to 200 ha. These areas have a temperate climate with mean annual rainfall ranging from 590 to 620 mm (BOM 2013c, 2013d). Native vegetation in the Warby–Ovens National Park is dominated by granitic hills woodland with common overstorey species including E. blakelyi and E. macrorhyncha. Historically, the area was cleared primarily for sheep and cattle grazing, but today horticulture (especially grape growing) has expanded substantially. Native vegetation within the Rutherglen study area is predominantly box–ironbark forest (including E. macrocarpa, E. polyanthemos, E. tricarpa and E. sideroxylon), and the district is one of the major wine-growing regions in Australia. The final land use surveyed was eucalypt woodlots grown commercially for firewood on properties surrounding Chiltern (36
090 6800 S, 146
580 6200 E), north-east Victoria. Eight woodlots were surveyed (tree age 10–20 years; woodlot size 12–42 ha) of various tree varieties including E. saligna, E. grandis, E. globulus, E. camaldulensis and E. melliodora. These woodlots comprised a eucalypt overstorey, often with a mid-storey of shrubs (mostly acacias) and a ground layer of introduced grasses. We did not identify flowering of eucalypt species during our surveys. Regional climate is temperate and the mean annual rainfall is 587 mm (BOM 2013e). The most common native vegetation type in the study area is box–ironbark forest. Most farming in the district is focussed on wool and meat production, but some farmers are growing eucalypt woodlots to diversify their income. Field sampling Birds were surveyed in 30  200-m line transects in each land use/study area (i.e. a total of 120 transects) by a single observer. A minimum of 500 m was maintained between each transect to improve the independence of samples. Each transect was surveyed for 20 min using distance sampling methods, whereby the distance from the observer to sighted birds was recorded to allow bird abundance to be calculated, correcting for differences

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in detectability among species and sites (Buckland et al. 2001) (see ‘Calculating species and functional diversity’ below). The distance between crop rows at each site was measured before bird surveys to improve the accuracy of observer-to-bird distance estimates from the centre line of transects. Surveys began at sunrise and were completed by 1000 hours on days without strong winds or heavy rain. All species seen or heard in front of the observer (to avoid double counting the same individual) and less than 20 m above the tree canopy were recorded. Abundance measures were based only on those individuals sighted. Almond, apple and vineyard transects were surveyed at the following stages of crop development: flowering and/or earlyfruiting, late-fruiting, and post-harvest. Pilot surveys indicated that bird activity was very low outside these times (e.g. during dormant crop stages). Apple and vineyard transects were surveyed three times and almond transects were surveyed four times as part of a larger study on bird use of almonds (see Luck et al. 2013c, 2014). Eucalypt woodlots were surveyed in spring, summer, autumn and winter. Calculating species and functional diversity Species diversity and community composition As survey effort among land-use types varied slightly, we based species richness and abundance comparisons among land uses on mean values (number of species or number of individuals per transect per survey) to account for differing survey effort. These results were qualitatively similar to analyses based on total species richness. Also, we calculated expected species richness (and confidence intervals (CIs)) in each land use based on abundance data using the Chao 1 estimator (Chao 1987) in the software program EstimateS (Colwell 2013). This, and rarefaction curves from EstimateS output, gave an indication of potential undersampling of particular land uses. Species diversity was calculated using Shannon’s diversity index (Shannon 1948). Raw bird species abundance data were adjusted using Distance sampling software (ver 5.0) to calculate a corrected measure of abundance in each transect (Thomas et al. 2006). This takes into account differences in detectability among transects and land-use types. The decline in detectability with distance was modelled using the following candidate models: uniform with cosine expansion; uniform with simple polynomial expansion; half-normal with hermite polynomial expansion; and hazard-rate with cosine expansion (see Buckland et al. 2001; Luck and Smallbone 2011; Luck et al. 2013a for details). The model with the lowest Akaike’s Information Criterion value was chosen as the best model for calculating a global density estimate. This was then used to correct raw abundance data to bird abundance per 2-ha transect (i.e. density). Mean abundance was then calculated by summing the total abundance across all species in each transect and dividing by the number of surveys conducted (i.e. we calculated abundance per survey because the number of surveys differed across land uses). Individual species occurrence and abundance were also examined by calculating the proportion of transects on which the species was recorded and the mean abundance of each species per survey, respectively. We used non-metric multidimensional scaling (NMDS) based on a Bray–Curtis dissimilarity matrix to

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graphically represent differences in bird species community composition among land uses. Functional diversity For each land use, we constructed a matrix comprising all bird species recorded in that land use, their abundance and the values of various functional traits for each species. Waterbirds and species that were recorded only once or twice during the entire survey period were excluded from the functional diversity analysis, as the focus here was on birds regularly recorded in woodland or agricultural habitats. These data were entered into the program FDiversity (Casanoves et al. 2011) to calculate the indices of functional richness, functional evenness, functional divergence, and functional dispersion. Functional richness is the number of different functional traits occurring in a community (Petchey and Gaston 2002). The measure is strongly positively related to species richness, but has been commonly used in past studies. Functional evenness is the level of evenness in the abundance of species with particular functional traits (Villéger et al. 2008). It has similar properties to the measure ‘species evenness’ and is constrained between 0 (low evenness) and 1 (high evenness). Using the trait ‘body mass’ as an example, a community comprising a few large bird species that are highly abundant and many small bird species that are rare would have lower functional evenness than a community where abundance is more evenly distributed across body mass sizes. Functional divergence is the distribution of trait values across trait space and is also constrained between 0 and 1 (Laliberté and Legendre 2010). In communities where trait values are more widely distributed (e.g. both very large and very small birds are included), the measure of functional divergence is higher than when the distribution of traits is more constrained (e.g. the community consists only of medium-sized birds). Finally, functional dispersion is the pattern of trait values within trait space measured as the distance to the centroid value (Laliberté and Legendre 2010). A community where trait values are all a similar distance from the mean or ‘centroid’ value yields smaller measures of functional dispersion than one where trait values occur at varying distances. The four measures of functional diversity were calculated in each instance for different trait combinations (whereby traits were not highly correlated) covering different aspects of bird ecology as follows: morphological traits (body mass, wing length, wingspan/body mass, bill length), reproductive traits (maximum life span, clutch size), and foraging traits (foraging behaviour, foraging location, foraging substrate and diet). Through this analysis, we determined whether bird communities in particular land uses were functionally diverse on the basis of morphology, reproductive strategy, and foraging strategy/diet. These factors are directly related to a species’ capacity to cope with environmental change (e.g. morphology, reproductive strategy) and contribute to various ecosystem functions (e.g. foraging strategy). The different measures of functional diversity capture different aspects of how traits are distributed within functional trait space. There is increasing recognition that functional diversity is a more appropriate measure than species diversity when interested in how species communities may impact on ecological functions

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Data screening indicated that some of our data did not approximate a normal distribution, and subsequent transformations did not improve the distribution. There is increasing support for using untransformed count data in ecological analyses (e.g. McArdle and Anderson 2004; O’Hara and Kotze 2010; Warton and Hui 2011) so we used untransformed data to analyse differences in species richness, abundance and diversity among land uses with the Kruskal–Wallis test, which is a non-parametric ANOVA-type analysis. When the value from the Kruskal–Wallis test indicated a significant difference across land uses, we conducted post hoc pairwise comparisons among land uses using the multiple-comparisons test described in Siegel and Castellan (1988, p. 213). We based our comparisons on mean richness and mean abundance because the number of surveys differed across land uses (almond orchards and eucalypt woodlots being surveyed four times, and apple orchards and vineyards being surveyed three times). In some analyses, certain transects were identified as outliers with extreme values. We ran these analyses with outliers included and excluded, but in all cases this did not lead to a qualitative change in the results or our conclusions. Therefore, we present only the results with the outliers included. The software program FDiversity uses an ANOVA-type test to determine whether there are significant differences in functional diversity (i.e. richness, evenness, divergence and dispersion) across treatments (i.e. land uses: Casanoves et al. 2011). Post hoc pairwise comparisons among land uses are included as part of this test, and we used these to determine significant differences in functional diversity between land uses. The NMDS analysis was conducted in Primer ver. 6 (Clarke and Gorley 2006). Results Species diversity and community composition Cumulative species richness across all surveys was highest in almond orchards (56 species), followed by eucalypt woodlots (55), vineyards (48), and apple orchards (35) (see Table S2 for species lists). Estimated species richness (based on the Chao 1 estimator) was 62 (CIs = 56–80) in almond orchards, 56 (55–62) in eucalypt woodlots, 49 (48–58) in vineyards and 37 (35–51) in apple orchards, suggesting that almond sites were likely undersampled, but reinforcing the result from the raw data that vineyards and apple orchards supported fewer species than almond orchards and eucalypt woodlots. Mean species richness differed significantly among land uses (Kruskal–Wallis test: c23 = 76.2986, P < 0.001), being highest in

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almond orchards and eucalypt woodlots and lowest in vineyards (Fig. 1a). Species richness across crop development stages or seasons was relatively similar for each land use except vineyards where richness was substantially higher after harvest (Table S3). Mean abundance of birds among land uses overall was significantly different (c23 = 11.3469, P < 0.01), and although almond orchards and eucalypt woodlots had the highest abundance, pairwise comparisons among land uses did not indicate that one land use had significantly different mean bird abundance to another (Fig. 1b). Species diversity differed significantly among land uses (c23 = 52.3727, P < 0.001), interestingly being highest in almond sites, but similar among the other three land uses (Fig. 1c).

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occurring in a particular system (Cadotte et al. 2011). For example, if a system supports a relatively high diversity of bird foraging traits it may indicate greater capacity for birds to contribute to a range of functions such as biological control of insect pests, pollination and seed dispersal. Values for each trait were obtained from a large database covering over 300 bird species that has been used in related publications (Luck et al. 2012, 2013b). A description of the traits used in the current study, and the primary or secondary sources from which trait values were obtained are included in Table S1 in the Supplementary Material (available online only).

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Land use Fig. 1. Differences in bird communities among land uses. (a) Mean species richness; (b) mean species abundance; (c) species diversity. Error bars show 95% CIs; different lower-case letters above columns indicate significant (P < 0.05) pairwise differences between land uses based on a multiplecomparisons test (same letters indicate no difference; there were no differences in mean abundance between land uses).

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The NMDS plot indicated separation of bird communities across land uses (Fig. 2). We calculated the number of individuals per survey and the frequency of occurrence of individual birds (proportion of 30 transects on which a species was recorded) to give an indication of how abundant and widespread, respectively, a given species was in each land use. The threatened eastern subspecies of the Regent Parrot (Polytelis anthopeplus monarchoides) was the most abundant bird recorded in almond orchards, followed by the Yellow Rosella (Platycercus elegans flaveolus) (Table 1). Both these species have been recorded eating almonds (Luck et al. 2013c) and were among the most abundant species in each crop development stage (Table S3). Insectivores were the most widespread species in almond orchards, with the

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Red-capped Robin (Petroica goodenovii), Rufous Whistler (Pachycephala rufiventris) and Yellow-rumped Thornbill (Acanthiza chrysorrhoa) being recorded in 90% of transects (Table 2). Introduced species were the most common and widespread birds in apple orchards, led by the European Goldfinch (Carduelis carduelis). Interestingly, only the Silvereye (Zosterops lateralis) and Common Starling (Sturnus vulgaris) are recognised pests of apples (see http://www.dpi.nsw.gov.au/__data/assets/pdf_file/ 0012/321204/IPM-for-australian-apples-and-pears-section-3.pdf, accessed 23 March 2015). The Common Starling was also common and widespread in vineyards (though not during the early stages of crop development) (Table S3), followed by the large omnivorous species Australian Magpie (Cracticus tibicen) and Little Raven (Corvus mellori) (Tables 1 and 2). Eucalypt woodlots tended to support smaller insectivores with the Weebill (Smicrornis brevirostris), Grey Fantail (Rhipidura fuliginosa), Superb Fairy-wren (Malurus cyaneus), Striated Pardalote (Pardalotus striatus), Yellow-rumped Thornbill and Willie Wagtail (Rhipidura leucophrys) being common and/or widespread. The abundance of particular species also differed substantially across seasons (Table S3). Functional diversity

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NMDS 1 Fig. 2. Results from the non-metric multidimensional scaling (NMDS), showing differences in bird community composition across land uses.

Across land-uses, functional richness differed significantly for morphological (ANOVA: F3,166 = 6.03, P = 0.001), reproductive (F3,166 = 29.76, P < 0.0001) and foraging (F3,116 = 46.09, P 0.0001) traits (Fig. 3a). For morphological traits, vineyards and apple orchards had significantly less functional richness than eucalypt woodlots and almond orchards. The functional richness of reproductive traits was significantly greater in eucalypt woodlots than other land uses, while for foraging traits, almond orchards had significantly more functional richness than other land uses, while eucalypt woodlots had significantly more richness than apple orchards and vineyards (Fig. 3a).

Table 1. The five most abundant bird species in each agricultural land use The number next to each species is the total abundance across all transects divided by the number of surveys, rounded to the nearest whole number. Scientific names and full species lists for each agricultural land use are included in Table S2 of the Supplementary Material (available online only) Almond orchards

Apple orchards

Vineyards

Eucalypt woodlots

Regent Parrot (90) Yellow Rosella (66) Yellow-rumped Thornbill (56) Red-capped Robin (54) White-winged Chough (34)

European Goldfinch (124) Silvereye (85) Straw-necked Ibis (69) Common Blackbird (47) Australian Magpie (30)

Common Starling (145) Australian Magpie (84) Little Raven (59) Eastern Rosella (48) White-fronted Chat (28)

Weebill (47) Australian Magpie (42) Grey Fantail (40) Superb Fairy-wren (40) White-winged Chough (39)

Table 2. The five bird species with the highest frequency of occurrence across all surveys in each agricultural land use The number next to each species is the proportion of 30 transects in which that species was recorded. Scientific names and full species lists for each agricultural land use are included in Table S2 Almond orchards

Apple orchards

Vineyards

Eucalypt woodlots

Red-capped Robin (1.00) Rufous Whistler (0.97) Yellow-rumped Thornbill (0.90) Yellow Rosella (0.87) Australian Magpie (0.83)

European Goldfinch (1.00) Silvereye (0.93) Common Blackbird (0.87) Common Starling (0.60) Australian Magpie (0.57)

Australian Magpie (0.97) Eastern Rosella (0.77) Little Raven (0.73) Common Starling (0.57) White-fronted Chat (0.47)

Grey Fantail (0.97) Australian Magpie (0.90) Striated Pardalote (0.83) Yellow-rumped Thornbill (0.83) Willie Wagtail (0.77)

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Functional divergence of reproductive (F3,116 = 7.32, P < 0.001) and foraging (F3,116 = 7.36, P = 0.0001) traits differed significantly across land uses. For reproductive traits, apple orchards had significantly greater functional divergence than other land uses, while almond orchards had greater functional divergence than vineyards (Fig. 3c). The functional divergence of foraging traits was greater for vineyards than for other land uses. Functional dispersion of morphological (F3,166 = 4.24, P = 0.01), reproductive (F3,166 = 4.09, P = 0.01) and foraging (F3,116 = 4.02, P = 0.01) traits also differed significantly across land uses. For morphological traits, apple orchards had significantly greater functional dispersion than other land uses, and apple orchards and eucalypt woodlots had greater functional dispersion of reproductive traits than almond orchards. Eucalypt woodlots had lower functional dispersion of foraging traits than other land uses (Fig. 3d).

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Fig. 3. Differences in bird community functional diversity among land uses based on morphological, reproductive and foraging traits. (a) Functional richness; (b) functional evenness; (c) functional divergence; (d) functional dispersion. Error bars show 95% CIs; different lower-case letters above columns indicate significant (P < 0.05) pairwise differences between land uses (same letters indicate no difference; there were no differences in functional evenness for foraging traits or functional divergence for morphological traits).

Functional evenness differed significantly for morphological (F3,115 = 17.77, P < 0.001) and reproductive (F3,115 = 2.73, P = 0.05) traits, but not foraging traits (F3,115 = 0.24, P > 0.05). Apple orchards had significantly lower functional evenness of morphological traits than other land uses, while almond orchards and vineyards had significantly greater functional evenness of reproductive traits than eucalypt woodlots (Fig. 3b).

Different types of agricultural land uses supported different bird communities. Almond orchards had similar cumulative species richness to eucalypt woodlots, and mean species richness for these two land uses was significantly higher than for vineyards and apple orchards. Moreover, almond orchards had significantly higher species diversity than the other land uses, and our calculations of estimated species richness suggested that almond sites were relatively undersampled compared with eucalypt woodlots, vineyards and apple orchards. These results appear surprising given that almond orchards are less similar to native vegetation than eucalypt plantings. We expected eucalypt woodlots to support the most species and highest diversity. The patterns we observed are likely influenced by a combination of local-scale and broader-scale factors. Local-scale factors that influence bird species richness and community composition in agricultural landscapes include vegetation structure and complexity, tree density and resource availability (e.g. Hurlbert and Haskell 2003; Kavanagh et al. 2007; Radford and Bennett 2007; Cunningham et al. 2008; Bridle et al. 2009). Also, crop irrigation may increase productivity and inflate animal species richness in agricultural land uses (Hugo and van Rensburg 2008). All crop types (excluding woodlots) surveyed in our study were irrigated, so irrigation alone does not explain the differences in bird richness among crops. In north-west Victoria, almond orchards have two major food resource pulses: (1) a short, but intensive (i.e. relatively synchronous flowering over thousands of hectares) flowering period in late winter/early spring, and (2) almond nut development, which usually begins in October with mature nuts harvested in February/ March. Almond flowering may attract nectar-feeding birds, and almond orchards had the greatest number of honeyeaters of all land uses (n = 8) compared with eucalypt woodlots (n = 5) and apple orchards and vineyards (n = 2 for each). Almond flowering can also attract pollinating insects (Saunders et al. 2013), which in turn may attract insect-eating birds. Indeed, insectivores were some of the most widespread and abundant bird species in almonds throughout our survey period, suggesting that the crop supports insects at various stages of crop development. This is possibly related to the fact that almond growers do not spray

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pesticides because there are currently few insect pests of almonds. Conversely, pesticide application in apple orchards and vineyards is common (Department of Primary Industries 2013). Hence, it appears that crop-specific management practices can have dramatic impacts on bird communities using the crop. In almonds, the nut growth resource pulse lasts up to 6 months and provides an extensive and readily available food source for numerous species. A total of 11 parrot and cockatoo species have been recorded feeding on almonds, in addition to other species such as the Australian Raven (Corvus coronoides) and Little Raven that forage on almond debris on the ground (Luck et al. 2013c). Some of these species are considered major pests of almonds (Bomford and Sinclair 2002), though Luck (2013) demonstrated that almond-eating birds may also provide a benefit to growers by removing residual nuts left on trees after harvest that are susceptible to fungal and insect infestation (see below). Like almond orchards, apple orchards usually consist of a uniform stand of deciduous trees that have a flowering phase and a fruiting phase that may provide food resources for birds, but it appears that these resource pulses do not attract as many bird species. Parrots may consume apples (Ribot et al. 2011), but parrot species were not common or widespread in our orchards. The most abundant species was the European Goldfinch, a bird that primarily eats small seeds, but will take insects during the breeding season. Its commonness in apple orchards is surprising, but may be related to the weedy understorey that occurred in some of the orchards we surveyed. The major resource pulse for vineyards is fruit production, and while grapes are targeted by certain bird species (e.g. Common Starling and Silvereye), the vegetation structure of vineyards and resource availability does not appear to attract a large number of species relative to the other land uses we surveyed. Interestingly though, while species richness clearly differed among land uses, there was greater uncertainty about the difference in mean bird abundance, suggesting that the land uses we sampled may support similar numbers of individuals. This result is likely influenced by the high abundance of particular species that appear to specialise on certain crops. For example, the Common Starling, a major pest in vineyards (Bailey and Smith 1979; Bomford and Sinclair 2002), was highly abundant in our surveys often as a result of large flocks descending on grapevines, especially during the mature fruit and post-harvest stages of crop development (Table S3). Similarly, the European Goldfinch stood out as a highly abundant species in apple orchards, whereas abundance was more evenly distributed among various species in eucalypt woodlots and almond orchards (see Table 1 and Supplementary Material). Unlike the other land uses, eucalypt woodlots supported a high number of small insectivores, a result consistent with past studies in eucalypt plantings (Hobbs et al. 2003; Kavanagh et al. 2007; Loyn et al. 2007; Hsu et al. 2010) or revegetation or remnants in agricultural landscapes (Arnold 2003; Hannah et al. 2007; Martin et al. 2011). These species are commonly associated with eucalypt canopies and native shrubby understorey, which occurred in many of our woodlots. This is in comparison to the horticultural land uses that comprised simply an overstorey of the main crop (i.e. almond trees, apple trees or espaliered grape vines) and an understorey of either bare ground or primarily introduced grasses and herbs.

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At a broader scale, the different geographic locations of our study areas, landscape context or differences in the size of the regional species pool may explain our findings. Hunt (2013) surveyed birds in the largest patches of native vegetation near each agricultural study area (i.e. almond orchards: Hattah– Kulkyne National Park; eucalypt woodlots: Chiltern Box– Ironbark National Park; apple orchards: Shepparton–Mooroopna State Forest; and vineyards: Warby–Ovens National Park). These surveys found that Hattah–Kulkyne supported the highest species richness, suggesting that there may be a larger regional bird species pool, which may explain the higher number of species found in almond orchards. Also, proximity to native vegetation may explain differences in the richness and composition of bird species in agricultural areas, especially at critical times such as breeding (Fischer and Lindenmayer 2002; Haslem and Bennett 2008b), as may other differences among bioregions such as local climate. Further research is required to determine how adjacency to native vegetation influences bird use of different agricultural crop types. Patterns in functional diversity Functional diversity has been shown to decline with increasing land-use intensification (Flynn et al. 2009; Mayfield et al. 2010; Trindade-Filho et al. 2012; Luck et al. 2013b). In Australia, native vegetation generally supports higher bird functional diversity than does agricultural land uses (e.g. Fischer et al. 2007; Loyn et al. 2007; Barrett et al. 2008; Collard et al. 2009; Hanspach et al. 2011). However, our research indicates that it is important to be specific about the type of agricultural land use being studied because different types will be associated with different bird communities and the functional diversity of these communities may vary across land types. Functional richness is often positively correlated with species richness (Villéger et al. 2008) (in our study correlation coefficients were >0.6), so the functional richness of morphological, reproductive and foraging traits would be expected to be highest in eucalypt woodlots and almond orchards. This was generally the case, with a couple of exceptions. Eucalypt woodlots had the highest richness of reproductive traits of all land uses (including almond orchards). This may reflect the relatively high structural diversity of woodlot vegetation, which included an overstorey, shrub and grass layer, creating a variety of nesting options that would suit a broader diversity of species with different reproductive strategies. The shrub layer (or in the case of vineyards, canopy layer) is missing from the other land uses we surveyed. This relatively high structural complexity of vegetation would also explain the significantly higher functional richness of morphological traits found in eucalypt woodlots (Hanspach et al. 2011). Interestingly, almond orchards had a higher richness of foraging traits than eucalypt woodlots (and apple orchards and vineyards). This underscores the diversity of birds utilising this land use, ranging from nectarivores, aboreal and ground-foraging insectivores, granivores (including a rich diversity of parrots) and omnivores. This feeding diversity also likely contributed to the higher diversity of morphological traits found in almond orchards. Apple orchards had significantly lower functional evenness of morphological traits than the other land uses, suggesting that

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apple orchards were dominated by a few species with similar morphology. This result may have been influenced by the relatively high abundance of the European Goldfinch and Silvereye in apple orchards – both small birds with short bills. The agricultural land uses did not differ significantly in the functional evenness of foraging traits, indicating that there was similar abundance of birds in different foraging groups. This suggests that these land uses have the capacity to support more than just those species that might consume the crop. Functional dispersion of morphological traits was significantly higher for apple orchards than for the other land uses, while eucalypt woodlots had the lowest functional dispersion of foraging traits. Previous studies have found that functional dispersion (the pattern of trait values in functional space) generally increases with increasing land use intensity (Laliberté et al. 2010; Luck et al. 2013b). That is, more disturbed sites have higher measures of functional dispersion. This suggests that while disturbed sites are characterised by lower species richness, as was seen in the apple orchards, these species are actually quite functionally distinct though there are only a few species representing each functional type. Implications for ecosystem service provision, crop damage and bird conservation The type of birds using agricultural landscapes has important implications for crop production, and in certain circumstances bird conservation. Since the early 20th century, the literature on bird occurrence in crops has focussed mostly on birds as pest species inflicting crop damage (Triplett et al. 2012). Recently, attention has been drawn to the potential for birds to increase crop yields by, for example, assisting in the control of pest insect species in crops such as coffee and apples (Mols and Visser 2007; Karp et al. 2013). Bird activity in crops has the potential to yield both costs and benefits to growers, and a first step in understanding these trade-offs is to document the bird species that occur in particular crops, and the functional traits of those species, which dictate the types of behaviour the birds will engage in. In almonds orchards, growers are primarily focussed on those bird species considered pests because they consume nuts. This includes most of the parrot and cockatoo species we recorded during our surveys. Yet, Luck et al. (2013c) demonstrated that the damage associated with particular species can be spatially and temporally variable. For example, species such as the Sulphurcrested Cockatoo (Cacatua galerita) and Galah (Eolophus roseicapilla) can damage ~30% of nuts on a tree, but this damage is extremely localised, likely reflecting large flocks descending on a particular location. Conversely, species such as the Regent Parrot and Yellow Rosella damage fewer nuts per tree (~2%), but this damage is more widespread across orchards (Luck et al. 2013c). Moreover, the density of parrots in almond orchards can show interannual differences owing to yearly variation in environmental factors such as rainfall (Luck et al. 2013c). Our surveys were confined to a 12-month period and further research is required to examine longer-term trends in bird use of agricultural crops. While parrots and cockatoos are considered pests during almond nut growth, Luck (2013) demonstrated that these species can actually provide an ecosystem service to growers after harvest because the birds consume residual nuts in trees that are

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not collected as part of the harvesting process. These so-called ‘mummified nuts’ are susceptible to fungal and insect infestations, which may threaten future crop yields. Hence, by ‘cleaning up’ mummified nuts, birds are providing a service to growers by reducing the need to remove the nuts manually. Luck (2013) found that the monetary value of this service actually outweighed the monetary cost of bird damage to nuts prior to harvest. The relatively high abundance and frequency of occurrence of insectivores in almond orchards also suggests great potential for birds to contribute to biological control of insect pests. There are currently few recognised insect pests in almond crops. Yet, the Department of Primary Industries, Victoria, has recently identified Carob Moth (Ectomyelois ceratoniae) in almond orchards in north-west Victoria (see http://australianalmonds.com.au/industry/conference_2012/proceedings, accessed 23 March 2015). The Carob Moth is a globally significant pest known to damage a variety of crops ranging from dates to pistachios (e.g. Mehrnejad 2002; Nay and Perring 2005), and it represents a substantial emerging threat to the almond industry in Australia. The potential contribution of insectivorous birds in assisting with the control of this pest in almonds is a crucial area for future research. Common and widespread birds in apple orchards were either recognised pest species (e.g. Silvereye and Common Starling) or likely represented little threat to crop production (e.g. European Goldfinch and Australian Magpie). Interestingly, and a little unexpectedly, parrot or cockatoo species were not commonly recorded in our surveys, though they are recognised pests in apples (Ribot et al. 2011). Tree-foraging insectivores were not abundant or widespread in apple orchards, suggesting few opportunities for birds to contribute to insect pest control, and likely reflecting the fact that we worked in conventional apple orchards where pesticides are commonly used. However, Luck et al. (2012) found that the abundance of flycatchers (e.g. Willie Wagtail and Grey Fantail) within apple orchards increased with greater tree cover around the orchard. These bird species take insects on the wing and may help to control pests such as adult stages of Codling Moth (Cydia pomonella). This demonstrates that appropriate management of apple orchards and the surrounding landscape could improve the capacity for birds to contribute to ecosystem service provision (see Mols and Visser 2007). Pest bird species were also among the most common and widespread birds within vineyards, suggesting that growers face substantial challenges in limiting crop losses from bird damage. Yet, other bird species may help control the activities of pest birds in vineyards. For example, introduction of the New Zealand Falcon (Falco novaeseelandiae) into vineyards in New Zealand saw a 95% reduction in the number of grapes removed by introduced pest birds relative to vineyards without the falcon (Kross et al. 2012). In our study area, we recorded three raptors using vineyards: Brown Falcon (F. berigora), Nankeen Kestrel (F. cenchroides) and Black-shouldered Kite (Elanus axillaris). Further research is required into whether increasing the activity of these raptor species in vineyards (e.g. by providing suitable perching and nesting areas) can help to limit the impact of widespread pests such as the Common Starling and Common Blackbird. In most cases, the agricultural landscapes we surveyed supported common and widespread species. However, we also encountered threatened subspecies using particular crops. The

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most abundant bird species in almond orchards was the Regent Parrot, and the eastern subspecies of this parrot is listed as vulnerable, threatened or endangered across several states in its geographic range (Baker-Gabb and Hurley 2011). The role that almond orchards play in providing food for Regent Parrot populations is a crucial area for future research. The fact that this threatened subspecies is also considered a pest by growers mirrors the case of the endangered Baudin’s Black-Cockatoo (Calyptorhynchus baudinii) in Western Australia, which is considered a pest in apple orchards (Chapman 2007). In these circumstances, sensitive management approaches are needed to ensure that control programs do not impact negatively on the persistence of threatened birds. Further, it highlights how some agricultural land uses may contribute to species conservation if managed appropriately. Acknowledgements This work was funded by an Australian Research Council Discovery Grant (DP0986566) and Future Fellowship (FT0990436) awarded to GWL. We thank all the private land holders for allowing access to their properties to survey birds. Our research was approved by the Charles Sturt University Animal Ethics Committee (approval no. 09/123). Melanie Massaro and three reviewers provided valuable comments on drafts of the manuscript.

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