DOI: 10.5061/dryad.0k6djhb1n
title: Plausible causes of seed preferences and diet composition in seed-eating passerines

description: We evaluated whether seed mass, handling time, handling efficiency and
 profitability account for (a) preferences in controlled experiments, and
 (b) field-diet composition of four bird species of the Monte desert,
 Argentina. The question of whether birds maximise their energy intake
 rates while feeding on seeds is assessed. We used feeding experiments with
 six native seed species of 0.07 – 0.75 mg (i.e. the seed-size range
 consumed in nature), which account for 0.59 – 0.84 of the field diet of
 the four birds. We measured seed-handling times, and used published
 information on bird preferences and diets, and on seed chemistry, for
 further calculations. Bird preferences were always positively related to
 seed mass, and also to seed profitability in the two intermediate-sized
 birds. Diet composition correlated positively with seed mass and
 negatively with seed profitability in three species, but some birds also
 showed a flexible behaviour eating the most attractive seeds according to
 their availability. This behaviour is not genuinely opportunistic because
 it only focuses on a restricted fraction of the total seed species present
 in the field. Contrary to expectations of species coexistence due to
 resource partitioning, small and large birds showed similar feeding
 efficiencies when eating the smaller and the larger seeds. The positive
 association between seed mass and profitability in several studies
 suggests that most birds can maximise their energy reward, on average and
 in the long term, by preferring the larger seeds. A combination of
 potential feeding optimisation with certain flexibility in the field may
 characterise the feeding ecology of desert seed-eating birds.
description: <b>Seed species</b> Birds and
 seeds tested came from the Ñacuñán Biosphere Reserve (34°03’S, 67°54’W),
 Mendoza province, Argentina, which is in the central Monte desert and has
 been effectively excluded from domestic grazing since 1972. The climate is
 dry and temperate, with hot summers and cold winters. On average,
 &gt;75% of the annual rainfall occurs during the growing season
 (October–March; 273 ± 95(SE) mm, n = 47 yr). The main habitat type in the
 reserve is open woodland with dispersed <i>Prosopis
 flexuosa</i> and <i>Geoffroea decorticans</i> trees. The
 shrub stratum is dominated by <i>Larrea divaricata</i>, and
 the herbaceous stratum is mainly composed of perennial grasses and annual
 forbs (see Fig. S1, supplementary material). Seeds
 offered in the laboratory trials came from six herbaceous plant species
 that are common in the soil seed bank of the reserve (Pol et al. 2014).
 Four of them are from perennial C<sub>4</sub> native grasses
 (<i>Sporobolus cryptandrus</i>, <i>Pappophorum
 </i>spp., <i>Digitaria californica </i>and
 <i>Setaria leucopila</i>) and the other two are from annual
 native forbs (<i>Chenopodium papulosum</i> and<i>
 Parthenium hysterophorus</i>) (Table 1). The seed-size range (0.07–
 0.75 mg) offered was identical to the natural range of herbaceous seeds
 consumed by the birds in the reserve (Marone et al. 2008). The seeds used
 account for a high percentage of the granivorous fraction of the bird
 diets: 84% (<i>P. ornata</i>), 68 -77% (<i>Z.
 capensis</i>), 59-69% (<i>S. multicolor</i>), and 76-79%
 (<i>D. diuca</i>) (Marone et al. 2008, 2017). The grass seeds
 are protected by glumes and glumellas that surround the round (<i>S.
 leucopila</i>), oval (<i>S. cryptandrus</i>) or
 elongated (<i>Pappophorum</i> spp., <i>D.
 californica</i>) caryopses. The kernel of <i>P.</i>
 <i>hysterophorus</i> is surrounded by an achene or cypsela
 with two membranous glumellas, whereas the kernel of <i>C.</i>
 <i>papulosum</i> is suborbicular and covered by a thin,
 fragile membranous pericarp. Although the birds used in our trials always
 dehusk the seeds when feeding, eating the whole grain, most seeds of
 <i>S. cryptandrus </i>and <i>C.
 </i><i>papulosum</i> lose their seed coats during
 primary dispersal, arriving at the soil dehusked (L. Marone, pers. obs.)
 and so, we offered dehusked seeds of <i>S. cryptandrus </i>and
 <i>C. </i><i>papulosum</i> in our experiments.
 References to large and small seeds in the text correspond to seeds with
 high and low mass, respectively (Table 1) (see Fig. S2, supplementary
 material). <b>Seed-handling time
 experiments</b> We carried out
 handling-time experiments on <i>P. ornata</i>, <i>Z.
 capensis</i>, <i>S. multicolor</i>, and <i>D.
 diuca</i>, which differ in several body-size measurements (Table 2).
 Thirty-five individuals (8-10 for each species) were mist-netted in the
 Ñacuñán Reserve and kept in individual cages (30 × 20 × 20 cm) with a
 natural photoperiod for one week before the trials were carried out. At
 the lab, we provided all birds with commercial seeds (<i>Setaria
 italica</i> or <i>Phalaris canariensis</i>) and
 vitamin-enriched water <i>ad libitum</i>. The experiments for
 all the combinations of bird per seed species were made during the
 following 3-4 weeks to prevent captive individuals from becoming used to
 the laboratory diet (Cueto et al. 2001). After the experiments, we
 released all the birds in the same area where we caught
 them. Before each experiment, each bird
 was maintained without food for 2-5 hours. At the beginning of every
 trial, we moved one individual to an observational acrylic cage (40 × 40 ×
 40 cm) in darkness and, after one minute, the observer turned the light on
 and left the bird to feed for 10 min. In every trial, there were 50 seeds
 of one plant species on the ground of the cage. We assigned the order in
 which seed species were offered randomly, and we did not test the same
 individual with other seed species during the following 24 hs. Bird
 feeding activity was filmed using a video camera with a chronometer (±0.1
 s), at a velocity of 30 photograms per second. Images were digitalised and
 assessed using a photogram-by-photogram inspection. Handling time for
 seeds that disperse with husks was the interval from when the bird picked
 it up from the ground with its bill until it was peeled and swallowed
 (Benkman and Pulliam 1988). For seeds that disperse without any structures
 attached, handling time was the interval from when the seed was picked up
 until the bird started the head movement to search for another seed. Data
 were not collected when seeds were not eaten (Benkman and Pulliam 1988).
 Given that several seeds were usually eaten by the same individual during
 a trial, handling times were averaged for every individual and seed
 species. We used these averages to calculate bird species-specific mean
 handling time (n = number of individuals of a given bird species
 assessed). The calculation of seed handling time by the
 four seed-eating birds allowed us to estimate (a) seed handling efficiency
 (mg s<sup>-1</sup>), which is the amount of mass of each seed
 species incorporated by a given bird species per unit of time, and (b)
 seed profitability (kJ s<sup>-1</sup>), which is the energy
 that a bird species gains per unit of time when eating a certain food
 item. To estimate the profitability values, we used the calculations of
 the energy per unit of mass (kJ g<sup>-1</sup>) provided by
 seeds of every plant species, reported in Ríos et al. (2012). Seed masses
 used for these estimations were measured on dehusked seeds (Table
 1). <b>Bird-seed preferences and
 diet</b> Information on preferences for the
 six-seed species by the four-bird species comes from the published levels
 of seed consumption in a choice experiment (see Fig. 1 in Cueto et al.
 2006). In those experiments, we offered an equal number of seeds (20) of
 every plant species simultaneously, which were dispersed homogeneously on
 the experimental arena, avoiding the biases of uncontrolled studies (Díaz
 1990; Cueto et al. 2001). Seed preferences were established according to
 the mean proportion of seeds of each species consumed by each bird
 species. Field-bird diets in the Ñacuñán Reserve have been already
 published (see Table 2 in Marone et al. 2008), and are expressed as the
 proportion of the total seed mass eaten by each bird species that
 corresponds to each of the six plant-species evaluated.
 <b>Data analysis</b> Plausible causes of bird seed
 preferences and of the granivorous composition of the bird diets were
 explored by evaluating their relationship with four independent or
 “explanatory” variables (i.e. seed mass, seed-handling time, seed-handling
 efficiency, seed profitability) by using Generalized Linear Models (GLMs)
 with binomial distribution due to preferences and diets expressed as
 proportions (Crawley 2013). Each bird species was modelled in a separate
 GLM. Independent variables were standardized to make the estimates of the
 regression coefficients comparable, directly weighing the effect of each
 variable on the response. Variable selection was carried out by stepwise
 regression. The values of some of the independent variables were
 correlated according to the Spearman ordinal test: seed mass with
 seed-handling time in <i>P. ornata</i> (r = 0.94, p &lt;
 0.05), and seed mass with seed-handling efficiency in <i>S.
 multicolor</i> (r = 0.89, p &lt; 0.05), so we only retained one
 of the variables in the final models of both preference and diet to avoid
 problems with multicollinearity. In such cases, the variable with the
 highest standardized regression coefficient was retained (Montgomery et
 al. 2021). All statistical calculations were conducted in R with the ‘glm’
 function - ‘stats’ base package, and ‘stepAIC’ function - ‘MASS’ package
 (Venables and Ripley 2002).
 Different indicators of feeding efficiency may be
 used to assess whether birds fit model 1 or 2 for seed consumption: the
 time taken to deal with a food item (Grant et al. 1976), the number of
 seeds consumed per unit of time (Grant 1986), or the mass of seeds
 consumed per unit of time (Schluter 1982; Pulliam 1985). We assessed the
 way feeding efficiency of different-sized birds varies with small and
 large seeds using three indicators: handling time, handling efficiency and
 seed profitability, which made it possible to test the robustness of
 different indicators when the four bird species ate the smaller
 (<i>S. cryptandrus</i>, <i>C. papulosum</i>) or
 the larger seeds (<i>Pappophorum</i> spp., <i>S.
 leucopila</i>). As we were interested in contrasting feeding
 efficiency with the largest and smallest seeds, the two intermediate-sized
 seeds (<i>D. californica</i>, <i>P.
 hysterophorus</i>) were discarded for this analysis. The averages of
 each indicator for different bird species were compared with one-way
 ANOVA. Raw data were log-transformed on some occasions to accomplish ANOVA
 assumptions. Simple linear correlations reported in the text are always
 Spearman ordinal correlations.