selection of foraging sites by desert granivorous birds: vegetation structure, seed availability,...

7/29/2019 SELECTION OF FORAGING SITES BY DESERT GRANIVOROUS BIRDS: VEGETATION STRUCTURE, SEED AVAILABILITY, SPECIES-SPECIFIC FORAGING TACTICS, AND SPATIAL SCALE (rev

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Running head: Foraging by Desert Granivorous Birds1

2

SELECTION OF FORAGING SITES BY DESERT GRANIVOROUS BIRDS:3

VEGETATION STRUCTURE, SEED AVAILABILITY, SPECIES-SPECIFIC FORAGING4

TACTICS, AND SPATIAL SCALE5

6

FERNANDO A.MILESI1,JAVIER LOPEZ DE CASENAVE, AND VCTOR R.CUETO7

8

Desert Community Ecology Research Team (Ecodes), Departamento de Ecologa, Gentica y9

Evolucin, Facultad de Cs. Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires,10

Argentina11

12

13Corresponding author:14

Dr. Fernando A. Milesi15

Ecodes, Departamento de Ecologa, Gentica y Evolucin16

FCEyN, Universidad de Buenos Aires17

Piso 4, Pab. 2, Ciudad Universitaria,18

C1428EHA Buenos Aires, Argentina19


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ABSTRACT1

2

Seed availability in the algarrobal of the Monte desert, as in other deserts, is highly3

heterogeneous at small scales and associated with vegetation structure. Granivores are4

expected to show a selective use of space (within the capacities of their foraging techniques),5

resulting in a heterogeneous impact on the seed bank. First, this paper describes the foraging6

repertoire of granivorous birds in the algarrobal to develop predictions for their expected use7

of space. Although the granivory guild as a whole tracked the temporal availability of seeds,8

species within the guild differed in foraging behavior and seasonal changes. Then, selection of9

space by foraging birds was assessed through a two-scale bird-centered analysis, comparing10

the distributions of used and available sites. The guild of granivorous birds used the whole11

range of available micro-sites, though aggregating contrasting partial patterns. Micro-sites12

with more cover of shrubs, grasses and litter were preferred for pre-dispersal consumption,13

consistent with the frequent technique of attacking grasses from low woody perches. In14

contrast, micro-sites used for post-dispersal consumption did not differ from random,15

suggesting no safe micro-sites for seeds. At a bigger scale not particularly related to16

heterogeneity in food availability, a selective pattern was clearer: birds avoided meso-sites17

with low shrub and litter covers, far from trees. In conclusion, patterns are not straightforward18

and depend on considerations of spatio-temporal scale and species-specific characteristics.19


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RESUMEN1

Seleccin de sitios de alimentacin por aves granvoras de desierto: estructura de la2

vegetacin, disponibilidad de semillas, tcnicas de alimentacin especficas y escala espacial3

La disponibilidad de semillas en el algarrobal del Monte, as como en otros desiertos, es4

muy heterognea a escalas pequeas y est asociada a la estructura de la vegetacin. Se espera5

que los granvoros muestren un uso selectivo del espacio (dentro de lo que les permiten sus6

tcnicas de alimentacin) y en consecuencia tengan un impacto heterogneo en el banco de7

semillas. Primero, se estudi el repertorio de alimentacin de las aves granvoras para poder8

hacer predicciones apropiadas sobre su uso del espacio. Aunque el gremio de aves granvoras9sigui a la disponibilidad temporal de semillas, las especies dentro del gremio difirieron en su10

comportamiento de bsqueda de alimento y en sus cambios estacionales. Luego, se evalu la11

seleccin de sitios de alimentacin mediante un anlisis centrado en el ave, a dos escalas,12

comparando las distribuciones de sitios usados y disponibles. Todos los tipos de micrositio13

disponibles fueron usados por el gremio de aves granvoras, aunque con patrones parciales14

contrastantes. Los micrositios con mayor cobertura de arbustos, pastos y mantillo fueron15

preferidos durante el consumo predispersivo, de acuerdo con la tcnica frecuentemente16

observada de atacar pastos desde ramas bajas de leosas. En cambio, los micrositios usados17

para consumo postdispersivo no difirieron de lo esperado por azar, sugiriendo que no hay18

micrositios seguros para las semillas. A una escala mayor, sin una heterogeneidad importante19


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All organisms are distributed heterogeneously at some spatial and temporal scales; the1

interesting question is at which scales and why. Animals are expected to track variations in2

food abundance when these are coupled to perceptible environmental cues, as a consequence3

of evolutionary or behavioral processes (Klopfer and Ganzhorn 1985, Morrison et al. 1992).4

The resulting non-random patterns of association between intra-habitat characteristics and the5

activities of the animals are not only a consequence but also a potential cause of the6

heterogeneous distribution of resources (i.e. bottom-up vs. top-down effects).7

Many studies have sought bird-habitat relationships with vegetation as the main habitat8

factor, partly because birds strongly depend on plants for diverse activities (e.g. feeding,9

nesting, perching, refuge; see e.g. Cody 1985a, Verner et al. 1986). Sometimes vegetation is10

considered the proximate variable eliciting a selective response by the birds, but usually it is11

interpreted as a surrogate measure for correlated variables such as food abundance or12

predation risk that influence a fitness component (e.g. Pulliam and Mills 1977, Brush and13

Stiles 1986, Clark and Shutler 1999). It is not easy to distinguish the main resource causing14

selective patterns because many simultaneous factors are usually involved in habitat selection,15

probably acting at different scales (Johnson 1980, Hutto 1985). Moreover, observable patterns16

are constrained by experimental designs. Consequently, we consider it useful to study patterns17

of habitat selection with a priori hypotheses about the heterogeneity of the (main) causal18

factors and the possible responses of the focal organisms. It is also relevant to study the use of19


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marked preferences (e.g. Willson 1971, Marone et al. 1998b, Cueto et al. 2006).1

Consequently, granivorous birds are expected to forage according to seed availability,2

particularly if this is associated with detectable environmental cues, albeit constrained at3

ecological time scales by the repertoire of foraging tactics that allows them to detect and4

capture prey. Any selective and spatially non-random seed removal is then expected to affect5

the composition and spatial heterogeneity of the seed bank (Reichman 1979).6

The composition and spatio-temporal heterogeneity of the seed bank in the Monte desert of7

Argentina have been studied in detail (Marone and Horno 1997; Marone et al. 1998a, 2004).8

As in other deserts (Price and Reichman 1987, Kemp 1989, Guo et al. 1998), the abundance9

of seeds in the soil is very heterogeneous at the scale of centimeters to meters and strongly10

associated with the presence of vegetation and of litter on the ground. In general, there are11

many more seeds on the ground under woody cover, where litter accumulates (see details in12

Methods, below). These environmental differences are sufficiently clear-cut to predict that13

birds should be using them as cues to forage efficiently for seeds, showing a stereotyped14

pattern of higher or exclusive use of micro-sites with woody plants and litter. However, the15

patterns of seed abundance on the ground may alternatively be interpreted as the consequence,16

instead of the cause, of consumption by birds (Smith and Rotenberry 1990, Russell and17

Schupp 1998). Most loss of grass seeds from the seed bank is due to granivory and birds are18

the main granivores in autumn and winter (Lopez de Casenave et al. 1998; Marone et al.19


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The objective of this study is to quantify the use of space by granivorous birds relative to1

the spatial heterogeneity of the vegetation and the associated availability of seeds, considering2

spatial scale and species-specific foraging techniques. The first part describes the substrate-3

specific foraging behaviors of the main granivorous bird species of the Monte desert. This4

information is combined with previously acquired knowledge of the spatio-temporal5

availability of seeds, to predict space use by foragers according to spatial scale and foraging6

behavior. The second part uses a new set of observations of birds foraging for seeds to test the7

predictions by comparing random and bird-centered sites with two grain sizes (micro-sites8

and meso-sites). Finally, we discussed the relationship space use, seed availability and9

vegetation structure in terms of bottom-up vs. top-down effects, foraging behavior and spatial10

scale.11

12

METHODS13

Study area.The study was carried out in the Biosphere Reserve of acun (3403S,14

6754.5W), located in the central Monte desert, Province of Mendoza, Argentina. The15

climate is dry, with a mean annual precipitation of 349 mm (n = 31 years, 19722002) but16

with large among-year variations (193585 mm). It is also highly seasonal, with warm and17rainy summers (>20C; 269 mm) and cold and dry winters (< 10C; 80 mm). For a complete18

description of the study area see Lopez de Casenave (2001).19


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perennial grasses (Pappophorum spp., Trichloris crinita,Digitaria californica,Aristida spp.,1

Setaria spp., Sporobolus cryptandrus) since most of the reserve has been closed to cattle2

ranching and other significant human activities in 1971. About a third of the surface of the3

algarrobal lacks perennial vegetation, in the form of different-sized (from centimeters to4

meters) open patches. Forb cover varies strongly among seasons and years, usually an order5

of magnitude lower than grass cover. Forbs were not considered in the description of the6

vegetation structure, following local studies of the seed bank (Marone and Horno 1997,7

Marone et al. 2004).8

Seeds of herbaceous plants are the staple diet of granivorous birds (7599% of their9

granivorous diet is made of grasses and one forb; Lopez de Casenave 2001). Their abundance10

is very heterogeneous at small scales in the soil, with patches of extreme abundances close in11

space. Seeds are consistently more abundant under trees and shrubs and in depressions of the12

soil (Marone et al. 2004), where litter accumulates. Forb seeds form a persistent seed bank,13

and are the main cause of this pattern. The abundance of grass seeds is less heterogeneous,14

with some inter-annual variability. Forbs start producing seeds in the spring and grasses15

usually in summer, with summer and early autumn providing the richest availability of seeds16

on plants. Primary seed dispersal starts in late spring and finishes by winter; maximum seed17availability in the soil occurs during autumn and winter, and minimum at the start of summer18

(Marone et al. 1998a, 2004).19


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Lopez de Casenave 2001). Birds were observed with binoculars as long as they remained in1

sight (usually


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woody plant), (2) only where a herbaceous plant occurs (e.g. glean to herbaceous plant), or (3)1

may occur in patches without vegetation (e.g. glean to ground).2

3

Selection of foraging sites.A bird-centered analysis (Larson and Bock 1986) was used to4

evaluate the selection of foraging sites, comparing the characteristics of perennial vegetation5

around sites where granivorous birds were detected foraging (= use) with those of sites6

randomly located in the same area (= availability). This is a frequently used approach in7

multiscale studies of habitat selection by birds, usually associated with multivariate statistical8

analyses, with similar or different variables estimated at each scale. In this study, the9

comparisons were made simultaneously at two spatial scales: micro-sites (1-m radius), a scale10

associated with a strong heterogeneity of the seed bank, and meso-sites (10-m radius), a scale11

with environmental heterogeneity caused by tall trees (algarrobos). Using spatial ecology12

jargon, this is an analysis at two different grain sizes with the same extent (i.e., the algarrobal13

habitat).14

In sampling carried out independently from that of the previous section, foraging15

granivorous birds were sought with the help of binoculars by walking a set area of algarrobal16

in an approximately random way. We assumed that the probability of detecting a foraging bird17in a particular place is proportional to the amount of time that it spends searching and18

removing seeds there, providing evidence on its proportional use of foraging habitat. The spot19


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between November 1996 and August 1997. Bird observations and vegetation measures in the1

used sites were obtained seasonally between February 1997 (especially after May 1998) and2

February 2000.3

The vegetation at each site was characterized using a point-interception technique. At the4

micro-site scale, a thin aluminum pole marked at 25-cm intervals was erected every 10 cm5

along four radial 1-m length transects oriented to each cardinal direction (= 40 points per6

micro-site). At each point, perennial plants (trees, shrubs and grasses) touching the pole in7

every 25-cm interval up to 3 m height (and in the highest interval if at >3 m height) were8

identified to genus level. The presence of dense litter (obscuring the mineral soil beneath it) or9

its absence (bare soil) was also recorded. Several variables were calculated from these10

measurements: percentage cover per plant group (grasses, standing dry grasses, low shrubs,11

tall shrubs, and trees), percentage cover of bare soil and of deep litter, vertical density per12

stratum (number of 25-cm intervals with vegetation), absolute maximum height, mean13

maximum height and coefficient of variation of the maximum height. A similar set of14

variables was estimated at the meso-site scale by placing the vertical pole at 20 random points15

along four 10-m long radial transects in each cardinal direction (= 80 points per meso-site).16

The distance between the center of the meso-site and the canopy of the closest tree was also17measured.18

The procedure to evaluate selection started by detecting the main characteristics defining19


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(eigenvalue >1), the broken-stick model, and the scree-plot (Jackson 1993), always retaining1

>75% of the variability in the correlation matrix. Some variables were transformed (arcsin,2

square root or logarithm) to normalize their distributions and then standardized, and Varimax3

rotation of the axes was applied; the structure was robust anyway, as every axis was strongly4

correlated (Pearson correlation: P < 0.001) with its version in analyses without5

transformations or rotation. The distribution of the 60 randomly located sites in the6

multivariate space of the retained axes was considered as representing the availability or total7

environmental variation at that scale. Used sites (i.e. where a bird was foraging) were8

located in PCA multivariate space by calculating their scores from the matrices of eigenvalues9

and eigenvectors (see Rotenberry and Wiens 1998). Selection was analyzed with a graphical-10

spatial technique and with a more traditional statistical one.11

The graphical-spatial test consisted in representing used and random sites in scatterplots of12

the retained PCA axes and evaluating the relationship between the two classes of points with a13

multidimensional analysis of space segregation. This is a modification of a spatial analysis on14

a point pattern that classifies each point by its type and that of its nearest neighbor and15

compares the proportion of each kind of pair with that expected by chance. Generically, this is16

a join-counts analysis of a binary label according to a nearest-neighbor matrix, testing for17differences against a random labeling model (Dale et al. 2002, Fortin and Dale 2005). If used18

points are aggregated or if there are available zones where there is no use (i.e., random points19


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P. Dixon (http://www.public.iastate.edu/~pdixon/Splus/) to a multidimensional case, with the1

matrix of Euclidian distances between points and the identification of nearest neighbors2

obtained by programming a small routine in Visual Basic for Applications 5.0 (MS Excel 97).3

Two-tailed Kolmogorov-Smirnov tests for continuous samples (Siegel and Castellan 1988)4

were used to evaluate selection on each of the principal components by testing the null5

hypothesis that the two samples (used vs. available) come from the same population (= no6

selection). It is sensitive to differences in parameters of both central tendency and dispersion,7

so it can properly evaluate selection consisting in a skewed use of lower or higher values of8

some environmental variable (resulting in lower or higher mean or median) and selection9

consisting in avoiding extreme or central values (lower or higher dispersion, respectively; see10

James and McCulloch 1990, Clark and Shutler 1999, Hirzel et al. 2002).11

12

RESULTS13

14

Foraging behavior.A total of 1074 foraging sequences (consisting of 3,289 foraging15

events) of individuals of the six main granivorous bird species were recorded (Table 1). Most16

foraging attempts were on seeds, with considerable proportions of both post-dispersal and17pre-dispersal seed predation (Fig. 1). Although their repertoire of foraging maneuvers was18

wide, three behaviors clearly predominated when foraging for seeds: picking up seeds from19


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(Fig. 1a), tracking the seasonal variations in their availability in the environment compared to1

alternative resources as fruits and insects. Similarly, pre-dispersal seed predation was higher2

in summer and autumn, after the production of new seeds, and decreased after the primary3

dispersion season (Fig. 1b).4

All the patterns at the guild level were substantially different between bird species.5

WhereasZ. capensis, D. diuca and Phrygilus carbonarius (Carbonated Sierra-Finch) used6

mainly the ground as foraging substrate, foraging individuals ofPoospiza torquata (Ringed7

Warbling-Finch) avoided the ground and just one quarter of the attacks were on seeds. This8

species showed a wider repertoire of behaviors, and switched foraging strategies between9

seasons: in spring and summer it fed mainly by gleaning from the foliage in higher strata (>110

m high), and during the non-breeding season it increased the consumption of pre-dispersal11

seeds from herbaceous plants (Table 1). The two remaining species, Saltatricula multicolor12

(Many-colored Chaco-Finch) and Poospiza ornata (Cinnamon Warbling-Finch), had13

characteristics between those extremes.14

The differences in maneuvers and substrates used by these birds allow for a better15

prediction of their use of space at small scales (micro-sites) when foraging for seeds (Fig. 1b).16

Pre-dispersal seed predation must be constrained by the availability of a non-woody plant17(usually a grass) with seeds, restricting the usable micro-sites in space and time (between seed18

production and primary dispersal). Moreover, the technique of removing seeds while perching19


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grasses and litter, because they have more seeds in the ground and usually allow for pre-1

dispersal seed predation too.2

3

Availability of foraging sites.At the micro-site scale, the first three principal components4

retained 77.4% of the variability in the matrix from the 16 variables considered in the 605

randomly located micro-sites (Table2). The first component (PC1) represents the general6

cover of vegetation, with positive values associated with shrubs, cover density under 2 m7

height and mean height of vegetation, and negative values associated with the absence of8

vegetation and higher variation in vegetation height. Ground cover also appears in this9

component, with dense litter cover on the positive values. PC2 represents the cover of trees10

and its effect on density of vegetation above 2 m and maximum height. In PC3 the rest of the11

perennial vegetation is represented: grass cover and its influence on vegetation density in the12

lowest stratum. There were no significant differences between the micro-sites measured in13

different seasons in any of the three components (KruskalWallis tests, k= 4, n = 60; PC1:H14

= 2.18, P = 0.54; PC2:H= 1.54, P = 0.67; PC3:H= 1.21, P = 0.75), confirming that this15

characterization of perennial vegetation is relatively constant throughout the year and16

allowing the use of all micro-sites together as an estimation of availability. The most17important variables in the first two axes (PC1: shrub cover and litter; PC2: tree cover) were18

those used in previous studies to describe the variability of the seed bank at the microhabitat19


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The interpretation of the axes is similar to that of the micro-site scale. The only relevant1

difference was the cover of low shrubs appearing in PC3 in the positive values, and grasses in2

the negative. Again, there were no differences between measurements made in different3

seasons (Kruskal-Wallis tests, k= 4, n = 60; PC1:H= 5.03, P = 0.17; PC2:H= 1.64, P =4

0.65; PC3:H= 2.65, P = 0.45).5

6

Selection of foraging micro-sites.We measured 85 micro-sites and 80 meso-sites for 887

foraging individuals detected. As expected, the number of observations of foraging birds was8

very variable among species, seasons and type of consumption, matching the general patterns9

shown in the previous section (Table 3). The most frequent species were Z. capensis10

(particularly during autumn-winter) and S. multicolor; P. ornata was absent in winter, and P.11

torquata only foraged for seeds when available on the plants. Pre-dispersal seed predation was12

lowest in spring and post-dispersal in summer. Observations ofP. torquata seed predation13

were all of pre-dispersal, whereas almost all those ofZ. capensis were post-dispersal, with S.14

multicolorand P. ornata intermediate. A few observations by other species were only15

considered at the guild level.16

Considering the whole guild, no area in the multivariate space of PC13 was left unused by17

the foraging birds (Fig. 2a). There was no evidence of spatial segregation of used and18

available points in the PCA three-dimensional space (test of spatial segregation by19


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As expected after the results of foraging behavior, the use of space by the whole guild1

aggregates contrasting species-specific patterns, particularly the proportion of pre-dispersal2

vs. post-dispersal seed foraging. In fact, there was a tendency for spatial segregation in the3

three-dimensional PCA space between both kinds of seed predation (C= 4.709, P = 0.095;4

Zpre = 1.626, P = 0.103;Zpost= 1.626, P = 0.053, Fig. 2a). During pre-dispersal seed predation,5

the use of micro-sites was highly skewed towards those with high woody cover and litter6

(PC1) and grasses (PC3; Fig. 3). Used micro-sites during post-dispersal seed predation, in7

contrast, did not differ from a random sample of those available, except for a tendency in PC18

for a lower variability caused by the exclusion of micro-sites with the highest cover, where9

accessibility to the ground may be restricted. For example, there were no micro-sites used for10

post-dispersal seed predation with values >1.5 on PC1 (approximately equivalent to >55%11

cover of low shrubs, >58% of shrubs and >58% of dense litter), whereas 8% and 11% of the12

random and pre-dispersal ones, respectively, were in that category.13

The selection of micro-sites by each bird species was also consistent with expectations.14

The species of the genus Poospiza, doing only (P. torquata) or mostly (P. ornata) pre-15

dispersal seed predation from the low branches of shrubs and trees, restricted their foraging to16

micro-sites with higher cover of shrubs and low shrubs, dense litter and grasses, with a17

tendency in P. ornata for a higher mean value of tree cover (Fig. 3). In contrast,Z. capensis,18

almost exclusively post-dispersal, used the full range of micro-sites without showing a19


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0.333, P > 0.1), as inZ.capensis. Seasonal patterns (not shown) were just a consequence of1

bird species fluctuations in abundance and diet; for example, the use of space in summer was2

skewed because most observations were of pre-dispersal seed predation by P. ornata, whereas3

use in winter was not different from random, when most observations were of post-dispersal4

seed predation byZ. capensis.5

6

Selection of foraging meso-sites.In contrast with the results at the micro-site scale, there7

is a range of meso-sites available in the algarrobal that were not used for foraging by the8

granivorous birds (or their use was so rare that it was not detected in our sample; Fig. 2b).9

Unused meso-sites were those with low shrub cover (negative values of PC 1; Fig. 4). For10

example, 13% of available meso-sites and 2% of used had values on PC1 < -0.75 (c.f. 2% of11

the available and 17% of the used with values >2). Distributions of used and random meso-12

sites did not differ on the other two axes (Fig. 4) so no segregation in the PCA three-13

dimensional space was detected (C= 0.681, P = 0.650). This pattern of association between14

used meso-sites and higher horizontal and vertical cover did not depend on type of seed15

predation or species-specific characteristics (Fig. 4). Distributions of sites used for pre-16

dispersal and post-dispersal consumption did not differ in any axis (npre

= 38, npost

= 34, PC1:17

Dmax=0.214, P > 0.1; PC2:Dmax = 0.118, P > 0.1; PC3:Dmax = 0.245, P > 0.1).18

The distribution of distances to the nearest tree differed between used and random foraging19


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DISCUSSION1

2

As in other deserts, seed availability in the algarrobal of the Monte Desert is very3

heterogeneous at small spatial scales (Marone and Horno 1997; Marone et al. 1998a, 2004),4

and the variables that best characterize the heterogeneity of the vegetation are those associated5

with food abundance. Moreover, some evidence suggests that desert granivorous birds are at6

least occasionally limited by seed abundance (Pulliam and Enders 1971, Schluter and7

Repasky 1991, Repasky and Schluter 1994, Lopez de Casenave 2001). Although predictions8

of bottom-up spatial effects seem well founded, there is no straightforward pattern to the use9

of space by the overall guild of granivorous birds while foraging. The selective patterns10

detected in this study are explicable only after allowing for variations of scale, seasons, and11

species-specific characteristics of the birds.12

It is noteworthythat the guild as a whole tracks the seasonal availability of seeds (a13

bottom-up effect). Observations of granivory are more frequent when seed availability is14

higher, and the proportion of pre- vs. post-dispersal seed predation tracks phenology of seed15

production and dispersal. This should strengthen confidence in the predictions of bottom-up16

effects posed above. However, this guild pattern results from an eclectic and temporally17

variable combination of functional and numerical responses (changes in diet, foraging18

behavior and local abundance of species). Guild tracking of seed availability cannot be19


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consumers changes seasonally, because some are totally (P. ornata) or partially (Z. capensis)1

migratory, or change their diet (P. torquata; Lopez de Casenave 2001). Thus even though they2

have the same general diet, different species of granivorous birds perceive different patterns3

of spatial and temporal availability of seeds and have a different impact on the seed bank. In4

consequence, the species must be considered separately to properly evaluate bottom-up5

influences acting as selective processes, because an analysis at the guild level may blur or6

misrepresent those interactions (e.g., by averaging different responses, see Milesi et al. 2002).7

For example, heterogeneity of seed abundance in the soil may be important forZ. capensis but8

irrelevant for P. torquata. On the other hand, a guild measure that integrates all fluctuations9

throughout the year may facilitate building predictions to evaluate the top-down impact of10

birds as consumers.11

The use of space at small scales can be explained, at least for some species, by their12

foraging techniques rather than by the heterogeneity of seed abundance. Pre-dispersal seed13

consumption is spatially selective, although presumably not caused by (but perhaps correlated14

with) seed abundance in the ground. Foraging techniques of some species seem to constrain15

which seeds are accessible. In fact, seasonal changes of diet ofP. torquata may result from it16

keeping the same general foraging technique all year round (moving along branches of trees17

and shrubs), namely finding more insects during spring and summer and more seeds on18

herbaceous plants (mostly grass spikes reachable from low woody branches) in autumn and19


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Moermond 1990). The impact of pre-dispersal seed predation, mostly limited to summer and1

autumn, should decrease the proportional contribution to the seed bank of those plant species2

or individuals growing close to woody plants.3

Contrary to expectations based on the scale at which heterogeneity of seed abundance is4

higher, the clearest selective pattern of granivorous birds was detected at the meso-site scale5

(10 m radius). All granivorous species studied (and the guild as a whole) selected meso-sites6

with higher woody cover and litter, not far from trees (or avoiding those with the opposite7

features). We have no evidence of heterogeneity in the seed bank at this scale except as an8

extrapolation of what was found at smaller scales (e.g. a meso-site with high shrub cover must9

have more shrubby micro-sites). Any conclusion that granivorous birds are foraging10

preferentially in meso-sites with higher availability of seeds in the soil requires three caveats:11

(1) features at one scale did not behave as good predictors of those at the other (Pearson12

correlations between scores of the available sites in corresponding axes of PCAs at different13

scales had significant but low coefficients of determination:PC1: r2 = 0.17; PC2: r2 = 0.21;14

PC3: r2 = 0.21, n = 60); (2) variation in seed abundance at the meso-site scale should be15

smaller, as all meso-sites tend to have some proportion of every kind of micro-site; and (3) at16

the meso-site scale other factors are expected to be important in choosing a foraging area,17

such as perching sites or predation risk. In fact, higher cover of woody plants and presence of18

trees is usually associated with a decrease in the risk of predation of birds in heterogeneous19


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granivorous birds have also been found in other arid environments (Wiens 1985, Dean and1

Milton 2001). These variable patterns may result from the set of spatial and temporal scales2used to evaluate selectivity. For example, pooling of different sorts of meso-sites (e.g.,3

different distances from trees) may hide the selective pattern found.4

The patterns of space use by birds fail to match simple predictions built from systematic5

differences in the mean abundance of seeds in the soil and its strong association with6

environmental clues given by the vegetation and litter, even when they are tested with the7

appropriate group at the appropriate scale. Post-dispersal seed consumption occurs across the8

range of available micro-sites, with no detectable differences from chance expectation. The9

same pattern is observed inZ. capensis, mostly foraging seeds from the ground. Although not10

the most parsimonious explanation, this is to be expected if birds are trading-off higher costs11

when foraging where seeds are more abundant. Higher fitness costs due to predation risk are12

usually associated with open spaces (see references above), and consequently not a priori13

positively correlated with the abundance of seeds in this habitat. Open spaces also pose higher14

costs due to heat and water regulation, particularly in summer (Wolf and Walsberg 1996). In15

contrast, patches containing more seeds typically have them trapped in dense litter, where16

searching costs may be higher than in bare soil (Getty and Pulliam 1993, Whittingham and17

Markland 2002). Another possibility is that environmental cues are not sufficiently reliable to18

be used by the birds. If the relative quality of micro-sites changes frequently then animals19


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22

potentially very high profits in soil depressions that trap grass seeds during secondary1

dispersal.2In summary, use of space of granivorous birds when foraging in the algarrobal is species-3

specific and scale-dependent. At the guild level, granivory tracks seasonal changes in the4

availability of seeds through changes in abundance, diet or foraging behavior of the different5

bird species. Predictions based on the heterogeneity of the seed-bank are not matched in the6

non-selective exploitation of every type of micro-site available for post-dispersal granivory,7

whereas foraging techniques skew the use of space for pre-dispersal seed predation. A clear8

selective pattern appears at the larger scale of meso-sites, though not particularly related to9

heterogeneity in food availability. From the perspective of seed survival, herbaceous plants10

near shrubs and trees may suffer a larger impact before dispersal, and there are no granivore-11

free micro-sites after dispersal. Apart from specific results concerning granivory in the12

algarrobal of the Monte desert, this study draws attention to the complex interactions that13

should be considered when trying to test predictions related to predator-prey dynamics and14

top-down vs. bottom-up effects. Simple patterns may occasionally show up, but more15

frequently a complete understanding will come from integrating information at different16

levels of analysis and various spatio-temporal scales.17


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23

ACKNOWLEDGMENTS1

2We thank L. Marone for valuable guidance at different stages. E. T. Mezquida assisted in3

the field, and P. Dixon, N. Giannini and M. L. Guichn provided useful comments on earlier4

versions. C. P. Doncaster and a reviewer helped to improve the English. Research was5

partially financed by Aves Argentinas/AOP, CONICET, ANPCyT and UBACyT. CONICET6

of Argentina and the University of Buenos Aires provided institutional support. This is7

contribution number 56 of the Desert Community Ecology Research Team (Ecodes), IADIZA8

Institute (CONICET) and FCEyN (Universidad de Buenos Aires).9

10

LITERATURE CITED11

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Milesi et al. Selection of foraging sites

TABLE 1. Percentages of foraging behaviors observed in the six main granivorous bird species of acun in each season (Poospiza ornata is1

absent in winter and unusual in autumn). A behavioral sequence of an individual consisted in one to 10 foraging events. See text for an2

explanation of the behavioral categories. The substrate in which the bird was standing (or from which flight was originated) is indicated before3

the dash, followed by the substrate from which food was actually taken. GR: ground; HP: herbaceous plant (mostly grasses); WP: woody plant4

(shrubs and trees). +: observed with frequency < 0.5%.5

Zonotrichia capensis Saltatricula multicolor P. ornata Poospiza torquata Diuca diuca Phrygilus carbonarius

Behavioral category Win Spr Sum Aut Win Spr Sum Aut Spr Sum Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum Aut

Seeds

Post-dispersal

Glean GRGR 99 82 72 84 34 39 33 40 63 35 + 1 3 + 96 83 57 88 93 70 59 78

Pre-dispersal

Glean GRHP 7 4 3 11 22 8 27 3 3 1 4 1 4 8 5

Leap 3 5 1 10 14 6 4 2 1 2 7 5

Sally-step 2 3 3 1

Glean HPHP 1 2 32 5 3 4 39 1 1 11 2 6 11 14 4

Glean WPHP 4 7 9 4 21 38 6 17 58 14 13

Sally-hover WPHP 1

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Non-seedsa

Glean WPWP (3m high) 6 1 5 14 2 10 28 15 15 6 6 3

Sally-hover WPWP 4 +

Probe (into WP) 1

Sally-strike 2 1 3 1 + +

Number of sequences 94 34 48 94 21 20 52 41 28 45 40 143 98 69 57 52 18 63 17 9 7 24

Number of foraging events 446 107 179 348 86 53 96 129 90 162 74 259 187 213 272 165 82 177 39 29 29 67

a Most of the sequences were directed to insects (adults and larvae), fruits and buds.

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TABLE 2. Results of PCAs with the variables measured at randomly located micro-sites and1

meso-sites (1660 and 1560, respectively). The highest loadings in each of the first three2

components retained (PC 13) are shown in bold.3

Micro-sites Meso-sites

PC 1 PC 2 PC 3 PC 1 PC 2 PC 3

Grasses -0.021 -0.073 0.867 0.297 -0.482 -0.717

Standing dead grasses 0.006 0.117 0.559 -0.090 0.124 -0.695

Low shrubs 0.740 -0.029 -0.161 0.401 0.180 0.649

Shrubs 0.861 0.297 -0.017 0.854 -0.075 -0.064

Trees -0.116 0.773 0.211 0.212 0.873 0.124

No perennial cover -0.859 -0.309 -0.359 -0.924 -0.064 0.202

Bare ground -0.716 -0.287 -0.437

Dense litter 0.771 0.251 0.375

Density 2 m 0.286 0.833 -0.113

Density 23 m 0.223 0.898 0.073

Density >3 m -0.070 0.871 -0.010

Maximum (absolute) height 0.493 0.746 -0.111 -0.090 0.904 0.142

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TABLE 3. Number of observations of granivorous birds considered for analyses of use of space1

at scales of micro-site and meso-site (in parentheses when different), by species, season2

and type of seed predation (pre-dispersal or post-dispersal).3

Season Type of consumption

Total Autumn Winter Spring Summer Predisp. Postdisp.

Guild 82 (76) 24 (22) 27 (25) 13 (11) 18 38 38 (34)

Species

Z. capensis 26 (22) 11 (9) 13 (11) 1 1 2 24 (21)

S. multicolor 30 (29) 6 10 10 (9) 4 16 9 (8)P. ornata 11 1 - 1 9 8 3

P. torquata 12 7 2 - 3 11 -

Other 6 1 3 1 1 1 2

Type of consumption

Pre-dispersal 38 11 11 2 14

Post-dispersal 38 (34) 11 (10) 15 (13) 8 (7) 4

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FIGURE LEGENDS1

2

FIG.1. Percentages of foraging sequences (a) directed to seeds (black bars) vs. other food3

(empty bars, mostly insects and fruit) and (b) of post-dispersal (seeds from the ground: empty4

bars) vs. pre-dispersal seed predation (seeds from herbaceous plants: grey bars), per bird5

species and per season. Black diagonal lines indicate observations of pre-dispersal seed6

predation of birds perched on woody plants.7

8

FIG.2. Distribution of (a) micro-sites and (b) meso-sites of foraging granivorous birds9

(black circles: pre-dispersal consumption; grey circles: post-dispersal consumption) in the10

first three components of PCAs with the matrix of measured variables at each scale (see Table11

2) in 60 randomly located sites (empty circles). Axes scales are proportional to the percentage12

of the variance of the variables-sites matrix retained by each component (shown in the axes13

titles).14

15

FIG.3. Distribution of available and used micro-sites (by the whole guild, for pre-dispersal16

or post-dispersal seed predation, and by each bird species) on the first three components of a17

PCA (PC13) with measured variables in the randomly-located micro-sites (see Table 2). The18

principal variables associated with each component are indicated. Each box delineates 25-19

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FIG.4. Distribution of available and used meso-sites (by the whole guild, for pre-dispersal1

or post-dispersal seed predation, and by each bird species) on the first three components of a2

PCA (PC13) with vegetation variables in the randomly-located meso-sites (see Table 2).3

Annotations as for Fig. 3.4

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FIG.1.

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FIG.2.

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FIG.3.

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FIG.4.

selection of foraging sites by desert granivorous birds: vegetation structure, seed availability,...

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