TY - JOUR
AU - Guillette, Lauren, M
AB - Abstract Variation in animal material technology, such as tool use and nest construction, is thought to be caused, in part, by differences in the early-life socio-ecological environment—that is, who and what is around—but this developmental hypothesis remains unconfirmed. We used a tightly controlled developmental paradigm to determine whether adult and/or raw-material access in early life shape first-time nest construction in laboratory-bred zebra finches Taeniopygia guttata at sexual maturity. We found that juvenile access to both an unrelated adult and raw material of one color led to a majority preference (75%) by novice builders for this color of material over that for either natal-nest or novel-colored material, whereas a lack of juvenile access to both an unrelated adult and raw material led to a 4- and nearly 3-fold reduction in the speed at which novice builders initiated and completed nest construction, respectively. Contrary to expectation, neither the amount of time juveniles nor their adult groupmate spent handling the raw material appear to drive these early-life effects on zebra finches’ first-time nest construction, suggesting that adult presence might be sufficient to drive the development of animal material technology. Together these data show that the juvenile socio-ecological environment can trigger variation in at least two critical aspects of animal material technology (material preference and construction speed), revealing a potentially powerful developmental window for technological advancement. Thus, to understand selection on animal material technology, the early-life environment must be considered. INTRODUCTION The utilization of raw material from the surrounding environment for foraging, protection, and reproduction—hereafter, material technology—is widespread in animals (Hansell 2005; Lill and Marquis 2007; Shumaker et al. 2011). Examples of animal material technology include bower building, dam design, nest construction, tool manufacture and/or use, trap assembly, and shelter setup. In these examples, an animal must exhibit sufficient skill in, first, selection of appropriate raw material and, second, the technique(s) for the successful construction of the technology (Hansell 2005). Adverse consequences of variation in animal material technology range from loss of time (e.g., St Clair et al. 2018) and energy (e.g., Withers 1977), to missed foraging or mating opportunities (e.g., Farji-Brener 2003; Östlund-Nilsson and Holmlund 2003), and even, death (e.g., Damman 1987). Acquiring technological competence, then, is undoubtedly crucial in the life history of these animals (Bateson 1988). As developmental plasticity plays a ubiquitous role in shaping organismal phenotype (reviews in Taborsky 2017; Langenhof and Komdeur 2018), one relatively untested driver of technological competence may be the early-life environment in which an animal develops. Rich observational data suggest the early-life socio-ecological environment—who and what is around—interactively shapes material technology in animals (reviews of bird and primate data: Biro et al. 2006; Fragaszy 2011; Fragaszy et al. 2013; Meulman et al. 2013; Breen et al. 2016; Rutz et al. 2018), with the presence/behavior of experienced adults appearing to aid youngsters’ learning of “what to do.” For example, juvenile New Caledonian crows Corvus moneduloides are more likely to handle abandoned extractive foraging tools made by their parents than they are to handle tools made and abandoned by other adult crows (Holzhaider et al. 2010a); unweaned chimpanzees Pan troglodytes craft and use ant-dipping stick tools exclusively in the presence of their foraging, ant-dipping mother (Humle et al. 2009); and young Sumatran orang-utans Pongo pygmaeus abelii construct their first weight-bearing nest only after 3 years of adolescent exposure to nests constructed every night by their mother (van Noordwijk and van Schaik 2005). Together these data imply that animals combine relevant social and ecological cues from early life when developing their technological competence. Owing to ethical and logistical constraints on field experiments, however, it has remained difficult to determine experimentally whether adults and/or raw material affect the development of material technology in animals. And the majority of laboratory experiments to date—where the typical method has been to human-rear a group of subjects in isolation from adult conspecifics (Scott 1902, 1904; Verlaine 1934; Collias and Collias 1964; Kenward et al. 2005; Kenward et al. 2006; Videan 2006; Morimura and Mori 2010; but see Tebbich et al. 2001)—confound possible effects of early learning opportunity with possible developmental effects of rearing experience (e.g., developmental differences in brain morphology caused by parental isolation; Bogart et al. 2014). To examine the effects of the socio-ecological environment in early life on material technology in animals, then, a more tractable study system and approach would be useful. For decades, the zebra finch Taeniopygia guttata has played a key role in illuminating how the environment in early life shapes mate choice and song production in adults under laboratory conditions (reviews in Slater et al. 1988; Griffith and Buchanan 2010). The zebra finch is also becoming a useful model system to examine the effects of experience on construction behavior (Breen et al. 2016). Indeed, laboratory work has identified social and ecological factors such as, respectively, conspecific familiarity (Guillette et al. 2016) and raw-material properties (e.g., color, Bailey et al. 2015; length, Muth and Healy 2014; rigidity, Bailey et al. 2014) involved in shaping adult zebra finches’ nest constructions. The links between the early-life environment and phenotypic development in zebra finches suggest, then, that study on socio-ecological effects in early life on nest construction in zebra finches should not only be feasible—but also profitable. Consistent with the idea that the early-life socio-ecological environment plays a role in shaping zebra finches’ nest construction, observational data show that wild juvenile (i.e., fledged) zebra finches remain near to their parents for at least 30 days post-fledging (Zann 1996), potentially learning something of these experienced adults’ choice/effective handling of material if they breed again (wild pairs of zebra finches re-breed often, up to six times, back-to-back in a single breeding period; Zann 1996). That the juvenile socio-ecological environment may influence zebra finches’ early learning of nest construction is further suggested from experimental data showing that they appear not to imprint on natal-nest material (Sargent 1965; Muth and Healy 2012). Without appropriate controls, however, these imprinting results require verification. The aim of the current study was 2-fold: to determine whether the early-life social and ecological environment shape 1) material preference for and 2) speed at first-time nest construction (defined here as how quickly nest construction is initiated and completed) by laboratory-bred zebra finches. In this species, both the choice of material for and speediness at nest construction are particularly relevant breeding behaviors because, in the wild, zebra finches are nomadic and breed opportunistically; they need to readily identify suitable material and capitalize on a potential breeding opportunity (Zann 1996). To test the hypothesis that the early-life socio-ecological environment plays a role in the development of nest construction in zebra finches, we conducted a 2 × 2 factorial developmental experiment (Figure 1) in which we manipulated the social (provided access to an experienced nest-constructing adult conspecific: yes or no; A+ or A−) and ecological (provided access to non-natal nest material across twelve 1-h material experience sessions: yes or no; M+ or M−) environment of 32 juvenile (60–90 days post-hatch) nonsibling same-aged male–male pairs (because males are the builders in this species). At sexual maturity (90 days post-hatch), we then provided each of these males with a mate, a nestbox, and three material-types for first-time nest construction: material that matched in color 1) to their natal nest, 2) to their juvenile environment (where applicable), or 3) was novel. Inclusion of a novel material prevented forced binary choices—for males in the M+ treatments—between natal-nest material and colored material from the juvenile environment. To enable meaningful comparisons between experimental treatments, two of the raw-material options were novel for the males that had not had access to the material during the juvenile environment experimental phase (M− treatments). The first-time nest-construction behavior of all males—material preference and construction speed—was subsequently assayed from video recordings (see Methods for details). Figure 1 Open in new tabDownload slide Schematic of the experimental protocol. Males hatched into a (a) natal environment of either a nest built with pink or orange material (n = 16 males per material type), which we removed at ~23 days post-hatch. At 60 days post-hatch, males were placed in same-aged nonsibling pairs from natal nests of the same color and assigned to one of four (b) juvenile environment treatments (n = 8 males per treatment) for a 4 week period: A−/M−: no access to an adult or material; A+/M−: access only to an unrelated adult groupmate; A−/M+: access to two piles of either pink or orange material for 1 h, three times per week (12 times in total); A+/M+: experimental conditions were identical to treatment A−/M+ except that males also always had access to an unrelated adult conspecific. At sexual maturity (90 days post-hatch), the 32 males were paired with females (from the same natal environment), given a nestbox, and provided with three different types of colored material (n = 20 pieces per material type) for (c) first-time nest construction: 1) material that matched their natal environment, 2) material that matched their juvenile environment (where applicable i.e., M+ treatments), and 3) material that was novel (an opt-out option; two of these options were novel for males in M− treatments—this allowed for meaningful between-treatment comparisons). Figure 1 Open in new tabDownload slide Schematic of the experimental protocol. Males hatched into a (a) natal environment of either a nest built with pink or orange material (n = 16 males per material type), which we removed at ~23 days post-hatch. At 60 days post-hatch, males were placed in same-aged nonsibling pairs from natal nests of the same color and assigned to one of four (b) juvenile environment treatments (n = 8 males per treatment) for a 4 week period: A−/M−: no access to an adult or material; A+/M−: access only to an unrelated adult groupmate; A−/M+: access to two piles of either pink or orange material for 1 h, three times per week (12 times in total); A+/M+: experimental conditions were identical to treatment A−/M+ except that males also always had access to an unrelated adult conspecific. At sexual maturity (90 days post-hatch), the 32 males were paired with females (from the same natal environment), given a nestbox, and provided with three different types of colored material (n = 20 pieces per material type) for (c) first-time nest construction: 1) material that matched their natal environment, 2) material that matched their juvenile environment (where applicable i.e., M+ treatments), and 3) material that was novel (an opt-out option; two of these options were novel for males in M− treatments—this allowed for meaningful between-treatment comparisons). Our experimental design thus allowed us to test the following nonexclusive hypotheses and predictions: 1) males imprint on natal-nest material irrespective of the juvenile environment (if so, for construction of their first nest all males should prefer material of the same color as that of the nest into which each hatched); 2) juvenile experience of material alone is sufficient to shape a male’s material preference (if so, males provided access to material when juvenile—M+ treatments—should prefer this same color of material for first-time nest construction); 3) males integrate both juvenile social and ecological cues when developing their material preference (if so, then only those males provided with juvenile access to both an adult and material—A+/M+ treatment—should prefer this same color of material when they construct their first nest); finally, 4) speed at first-time nest construction is a result of an interaction between the juvenile social and ecological environment (if so, then those males that have had juvenile access to both an adult and material—A+/M+ treatment—should be the quickest to initiate and complete their first nest). METHODS Participants and husbandry Participants in the current study were 148 zebra finches (78 males; 70 females) bred at the University of St Andrews or obtained from a local breeder. Of the 148 zebra finch participants, 76 birds (38 males; 38 females) served as breeding pairs; 32 male offspring of the breeding pairs served as experimental subjects; 32 female offspring of the breeding pairs served as partners to the male subjects; and 8 additional males served as companions to half of the male subjects. Breeding pairs and companion males had all previously constructed at least one nest, whereas the male subjects and their female partners were naïve to nest construction. All birds were provided ad libitium access to food (Johnson & Jeff seed, oyster shell grit, calcium and vitamin block), egg mix for breeding pairs and young (up to 35 days post-hatch; Haith’s egg biscuit food), plus spinach three times per week and water (supplemented with vitamin D3 three times per week), and kept on a 14:10 light:dark cycle, with humidity and temperature levels at approximately 50% and 20° C, respectively. Prior to and following this study, birds were housed in same-sex colony cages (140 × 71 × 122 cm). Experimental apparatus and setup Twelve identical test cages (50 × 50 × 50 cm) were used to test all birds. Attached to the left and right front of each test cage were, respectively, a food and water hopper, in addition to two perches. On the floor of each test cage, the following items were placed: cuttlefish bone, oyster shell grit, vitamin block, and a food and water bowl. Two 2.4 GHz Bird Box cameras (Spy Camera CCTV) were wired to the roof of each test cage. One camera was focused on the cage floor and the second camera was focused on the nestbox (when one was present—see Experimental protocol). Both cameras were connected to one of four desktop computers or one of two laptop computers used to record birds’ behavior during testing as detailed below. Birds could hear but not see their neighbors as we placed an opaque white barrier between each test cage. See Supplementary Figure S1 for an image of the experimental apparatus and setup. Experimental protocol The experiment consisted of three phases (Figure 1): 1) natal environment, 2) juvenile environment, and 3) first-time nest construction. In each of these three phases, we used at least one of three different types of colored material: pink, orange, and white string (jute craft twine from James Lever Co., London, UK). All material was cut to 15 cm lengths. The material-types fall within the range of zebra finch color vision (Hart 2001) and were chosen based on our previous work (Bailey et al. 2014; Guillette et al. 2016; Breen et al. 2019), which shows that male zebra finches can discriminate between each of them. We used the in-cage cameras described above to record experimental phases (2) and (3). Natal environment Breeding pairs were each placed in a breeding cage (50 × 50 × 50 cm) for 6 days in order to form pair bonds. On the morning of the seventh day, pairs were provided with a wooden nestbox (11 ×12 × 4.5 cm) and material (either 400 pieces of pink or orange string cut to 15 cm lengths; n = 19 per string type) with which to construct their nest (males can construct a species-typical domed nest with this length and amount of material—see figure 2 in Breen et al. 2019). Nests were checked for eggs once per day until the first egg, after which, we removed any remaining material not in the nest (to prevent males from adding more material, which can result in the eggs being buried; Zann 1996). The nests plus nestboxes were removed 5 days after the first individual in a brood fledged (~23 days post-hatch). As zebra finch chicks do not necessarily fledge all at once (Zann 1996), this time window allowed for all young to leave the nest before we removed it. Fledglings remained with their parents until nutritional independence (~35 days post-hatch; Zann 1996), after which, we returned parents and any female offspring to the same-sex group housing conditions described above. Nutritionally independent subject males remained housed with brothers until the start of the next experimental phase. Where this was not possible (because parents produced a single male offspring), we added these single males to a family group of same-aged males and, when later paired (see Juvenile environment), treated these birds as if they were full brothers to prevent the pairing of two familiar individuals. None of the offspring hatched in the natal environment phase were able to observe nest construction as they did not have visual access of other birds outside their cage (because we placed an opaque barrier between each breeding cage). Throughout the natal environment experiment phase, we checked pairs once per day in order to gauge breeding progress. Juvenile environment Approximately 56 days post-hatch, juvenile subject males were placed in nonsibling same-aged male–male pairs matched for the natal environment (i.e., pink or orange natal nest) in a test cage and assigned to one of four treatments (Figure 1): 1) no access to an adult or material (A−/M−); 2) access to an adult but no access to material (A+/M−); 3) no access to an adult but access to material (A−/M+); and 4) access to both an adult and material (A+/M+). No juvenile birds were related to the adult males or had a brother in the same treatment. Considering genetic as well as other constraints (e.g., time, facility space, and equipment availability) in tandem with statistical power (Taborsky 2010), the sample size for each of the four treatments was thus eight birds (i.e., four juvenile pairs). Before we placed birds in their respective cages, we marked the top of their head (using a nontoxic and nonpermanent marker pen; Jiffy Eco-marker Ink) with a unique mark so that we could later readily identify (from videos) and score each bird’s material-handling time (see below) in this second experimental phase. Once in their cages, birds were given 3 days to adjust to their new environment. On day 4 in their testing environment, each bird experienced their first (of 12) material experience sessions (three sessions per week) at either 4 or 5 h (pseudo-randomized across sessions) post-light onset. During each material experience session, birds in M+ treatments were provided colored (pink or orange) material in two piles (n = 20 pieces in each pile) for 1 h, after which, we removed all of the material, whereas birds in the M− treatments were sham-treated—that is, the experimenter (A.J.B.) briefly placed their hand without material in the respective cages at the start and end of the hour to match the actions performed in the M+ treatments. The material during the material experience sessions for birds in the M+ treatments was always of an alternative color—either pink or orange—to their natal-nest material. Note that we did not know if/how the juveniles or the adults in the M+ treatments would interact with the material we provided, except that, as a female was not present, we did not expect the adults to construct a nest (subsequent video scoring confirmed this expectation). We returned adult males in both A+ treatments to group housing (see above) after the 12th and final material experience session. The juveniles remained in pairs for 4 days after completing the juvenile environment experimental phase. The purpose of this was to ensure that each subject reached sexual maturity (90 days of age) before being provided a mate and moving on to the third phase of the experiment. First-time nest construction Approximately 90 days post-hatch, we moved each of the 32 (previously juvenile) subject males into a new test cage and paired each with an unrelated, same-age female (matched for natal-nest material). Pairs were then left for five additional days to form pair bonds. On the sixth day, we attached a wooden nestbox (11 × 12 × 4.5 cm) midway along the back wall of each pair’s cage (Supplementary Figure S1). We then provided pairs with three different types of colored material for constructing their first nest: material that matched their 1) natal environment, 2) juvenile environment (for males in M+ treatments), or 3) was novel (an opt-out option to not assume a role for early learning). Thus, for males in M+ treatments the novel material was always the white string, whereas for males in M− treatments the novel material was always the white string as well as a non-white string type—either pink or orange string. We placed the three different types of colored material in three distinct piles (n = 20 pieces in each pile; that is, 60 pieces in total—this amount is sufficient to yield insights into experiential drivers of avian nest construction; Guillette et al. 2016; Guillette and Healy 2018; Breen et al. 2019) centrally on the cage floor and equidistant from one another. The material-color order was randomized across pairs. After placing the material, we did not disturb pairs for 3 h. Thereafter we visually checked the nestbox three times a day, beginning at light onset and continuing at 4-h intervals until the end of this final experimental phase. The first-time nest construction experimental phase began at 6 h post-light onset and ended once a male had moved all colored material into his nestbox, after which, we removed the nestbox plus material, and we returned pairs to their respective colony cages as described above. Data extraction and statistical analyses General We used Solomon coder (www.solomoncoder.com) set at a time resolution of 0.2 s for all behavioral scoring of video recordings in the current study, and we performed all statistical analyses in R (R Core Team 2017). We confirmed the goodness-of-fit (all P > 0.05) of our statistical models using the “testUniformity” function from the “DHARMa” package (Hartig 2017) on the scaled model residuals. Model significance was always assessed using Type II likelihood-ratio chi-square tests (Langsrud 2003) from the “car” package (Fox and Weisberg 2011). Video scoring of first-time nest construction To assay the first-time nest-construction behavior of males, we scored (blind to treatment) the recorded 32 videos from the first-time nest construction experimental phase. Specifically, we scored the following behaviors for each male: 1) latency (in seconds; here and elsewhere) to first handle material (by making initial bill-to-material contact) and 2) latency to initiate (by depositing a piece of material within the nestbox) and 3) complete first-time nest construction (by depositing the 60th piece of material within the nestbox). We were unable to score behavior (1) for five males because (a) the female deposited all of the material in the nestbox (one male in treatment A−/M+) or (b) the subject died after completing the juvenile environment experimental phase (one male in treatment A−/M−) or (c) the video prematurely stopped recording before first-time nest construction, rendering latency measures inaccurate (one male in treatment A+/M− and one male in treatment A−/M−) or (d) the camera was initially angled incorrectly, obscuring one of the piles of material from view (one male in treatment A+/M+). We were also unable to score behaviors (2) and (3) for reasons (a–c) for these same corresponding males. The final dataset thus contained a sample size of 27 (A−/M−, n = 6; A+/M−, n = 7; A−/M+, n = 7; A+/M+, n = 7) for behavior (1) and a sample size of 28 (A−/M−, n = 6; A+/M−, n = 7; A−/M+, n = 7; A+/M+, n = 8) for behaviors (2) and (3). We also scored the color of the first 20 pieces of material a male deposited in his nestbox to determine, as detailed below, each male’s preferred color of material for constructing his first nest. However, as explained above, we were unable to determine the material-color preference for two males, and for a third male in treatment A+/M−, because his video recording cut-out during first-time nest construction. The final dataset thus contained the material-color preference of 29 males (sample size per treatment: A−/M−, n = 7; A+/M−, n = 7; A−/M+, n = 7; A+/M+, n = 8). To determine males’ material-color preference, we ran a Monte Carlo simulation to create a distribution curve of the likelihood of depositing the same color of material (e.g., pink) across 20 trials in an environment where three colored raw-material options (pink, orange, and white) always exist. From this simulation, we established that any one of the three colored material-types deposited more than 10 times (out of the first 20) within the nestbox is significantly different from chance (P = 0.038)—in other words, preferred. We then applied this material-preference criterion (as we have done elsewhere; Breen et al. 2019) to the first 20 pieces deposited by each male in his nestbox when he constructed his first nest. Where this criterion was not met (n = 1), we assigned material-color preference based on which colored material a male first used in entirety (by depositing all 20 pieces of the colored material in his nestbox; which this bird did in 43 deposits). A posthoc Monte Carlo simulation confirmed that depositing all 20 pieces of one colored material across 43 trials in a three-material-option environment is significantly different from chance (P = 0.026). For details on each male’s material-color choices and preference, see Supplementary Figure S2. Early-life effects on first-time nest construction Material-color preference To determine the effect of the early-life environment on zebra finches’ preferred color of material for first-time nest construction, we first classified the material-color preference of each male into one of three categories: 1) preferred material that matched in color to the natal environment; 2) preferred material that matched in color to the one provided during the juvenile environment (where applicable i.e., M+ treatments); or 3) preferred material of a novel color. We then analyzed these preference data using binomial generalized linear models, as exhibiting a preference for a particular category of material effectively produces binary (i.e., yes or no) outcomes. Because the true probability of expressing a preference for any one of the three colored material-types made available to each male was 0.33 (and not 0.5 as specified by the binomial error structure of our models), Model 1–3, detailed below, should be considered conservative. Our first model (Model 1) tested if novice builder zebra finches prefer material of the color of their natal nest irrespective of their juvenile experience. The response variable for Model 1 was whether (yes or no) males in each of the four treatments exhibited a preference for natal-nest material; the predictor variables included juvenile adult presence (yes or no), juvenile material access (yes or no), and their interaction. Our second model (Model 2) tested if juvenile material access is sufficient experience to shape material preference or if an adult also needs to be present, for experimental subjects in the M+ treatments. The response variable for Model 2 was whether (yes or no) a male subject preferred material from their juvenile environment; the predictor variable was whether (yes or no) they were, as a juvenile, housed with an adult. Our third model (Model 3) interrogated, for scope, if the early-life socio-ecological environment influenced whether (yes or no) males in each of the four treatments exhibited a preference for a novel material—the dependent variable; the predictor variables for Model 3 were identical to those of Model 1 described above. Ideally, we would have included juvenile test cage as a mixed effect in the above models to account for repeated sampling within each juvenile rearing environment, but this was not possible because adding this additional term would result in model overfitting (i.e., too many model terms given the number of observations). Nevertheless, we are confident that our tightly controlled experimental setting (in terms of food/water availability, temperature, and so on) minimized any between-cage environmental variation in this juvenile, and in all other, experimental phases. Construction speed We specified Cox proportional hazards models (CPHMs) using the “coxph” function from the “survival” package (Therneau 2015) to determine whether juvenile access to an adult and/or material influenced the speed at which males (Model 4) initiated and (Model 5) completed the construction of their first nest, as survival models explicitly consider time-to-event data. The response variable for Model 4 was the time taken by males to make their first material deposit within their nestbox once the material was made available. We used this measure in Model 4 because 1) males did not differ in how quickly they first touched the material provided with their bill for first-time nest construction (i.e., there was no confounding effect of material neophobia on males’ latency to initiate nest construction; Supplementary Figure S3) and 2) the alternative measure available for testing (i.e., latency to initiate nest construction as measured from the initial handling of the material by males) reduced the sample size in the A+/M+ treatment by one due to an initially incorrect camera recording angle (see above). The response variable for Model 5 was the time taken by males to make their final (60th) material deposit within their nestbox as measured from their first material deposit. We used this measure in Model 5 to ensure any effect of treatment detected on the speed of first-time nest construction by males was not driven by variation in the time taken to initiate first-time nest construction. The response variable for both Models 4 and 5 excluded the time elapsed due to the lights being turned off; that is, when birds were asleep. The fixed-effects structure (i.e., predictor variables) for both CPHMs included juvenile adult presence (yes or no), juvenile material access (yes or no), and their interaction. The proportional hazards assumption (that the relative probability of an event is constant across time) was satisfied (P > 0.05) by both global CPHMs, which we tested using the “cox.zph” function from the “survival” package. RESULTS Full output from each model can be found in the Supplementary Material. Early-life effects on first-time nest construction Material-color preference The early-life environment influenced males’ material-color preference for first-time nest construction, an effect that was specific to the juvenile period of development. Specifically, if a male had had juvenile access to both an adult and material (A+/M+ treatment) the likelihood that he preferred to use material of the color of his natal nest—no male in the A+/M+ treatment did (Figure 2a, left panel)—decreased significantly (preference for natal nest versus other material across all treatments: adult access × material access term, χ2 = 4.90, n = 29, P = 0.027; Model 1). Furthermore, the majority (75%) of males in the A+/M+ treatment preferred, for their first nest, to use material that matched in color to that which they experienced in their juvenile environment, whereas only one male in the A-/M+ treatment (juvenile material access only) preferred to do so (Figure 2a, middle panel)—a significant between-treatment difference (preference for juvenile versus other material across M+ treatments: adult access×material access term, χ2 = 5.99, n = 15, P = 0.014; Model 2). Collectively these data thus support the hypothesis that juvenile male zebra finches integrate both early-life social and ecological cues concerning raw-material “suitability” (here, color) when developing their material preference. Figure 2 Open in new tabDownload slide Early-life socio-ecological effects on avian nest construction. (a) Top panel: the proportion of males (y-axis) in each treatment (all n = 7 except for the A+/M+ treatment where n = 8; x-axis) that preferred to construct their first nest with material that (left) matched their natal environment, (middle) matched their juvenile environment (if provided material as a juvenile; males in M+ treatments), or (right) was novel. Material preference (i.e., depositing >10 pieces of one type of material out of the first 20 deposits) was determined from Monte Carlo simulation—see Methods. (b) Middle panel: cumulative proportion of males (y-axis) to initiate (measured from when material was provided; x-axis) and complete (measured from nest-construction initiation; x-axis) nest construction in each of the four treatments (A−/M−, n = 6; A+/M−, n = 7; A−/M+, n = 7; A+/M+, n = 8). The steepness of each slope in the middle panel indicates the speed at which males in each treatment initiated and completed their first nest; a steeper slope indicates quicker speed. (c) Bottom panel: total amount of time (left) juveniles in the M+ treatments (n = 167 observations from 16 birds) and (right) adults in the A+/M+ treatment (n = 41 observations from four birds) spent handling material (y-axis) with their bill in each of the twelve 1-h material experience sessions (assayed from 190 and 48 h of juvenile and adult video recordings, respectively; x-axis), ruling out that adults 1) increase juvenile groupmates’ material handling and 2) handle material more than juvenile groupmates. Each symbol in the bottom panel represents a single observation (juveniles in A−/M+, open circle; juveniles in A+/M+, filled circle; adults in A+/M+, filled diamond); linear least-squares regression “trend” lines and 95% confidence intervals are plotted for each treatment. Figure 2 Open in new tabDownload slide Early-life socio-ecological effects on avian nest construction. (a) Top panel: the proportion of males (y-axis) in each treatment (all n = 7 except for the A+/M+ treatment where n = 8; x-axis) that preferred to construct their first nest with material that (left) matched their natal environment, (middle) matched their juvenile environment (if provided material as a juvenile; males in M+ treatments), or (right) was novel. Material preference (i.e., depositing >10 pieces of one type of material out of the first 20 deposits) was determined from Monte Carlo simulation—see Methods. (b) Middle panel: cumulative proportion of males (y-axis) to initiate (measured from when material was provided; x-axis) and complete (measured from nest-construction initiation; x-axis) nest construction in each of the four treatments (A−/M−, n = 6; A+/M−, n = 7; A−/M+, n = 7; A+/M+, n = 8). The steepness of each slope in the middle panel indicates the speed at which males in each treatment initiated and completed their first nest; a steeper slope indicates quicker speed. (c) Bottom panel: total amount of time (left) juveniles in the M+ treatments (n = 167 observations from 16 birds) and (right) adults in the A+/M+ treatment (n = 41 observations from four birds) spent handling material (y-axis) with their bill in each of the twelve 1-h material experience sessions (assayed from 190 and 48 h of juvenile and adult video recordings, respectively; x-axis), ruling out that adults 1) increase juvenile groupmates’ material handling and 2) handle material more than juvenile groupmates. Each symbol in the bottom panel represents a single observation (juveniles in A−/M+, open circle; juveniles in A+/M+, filled circle; adults in A+/M+, filled diamond); linear least-squares regression “trend” lines and 95% confidence intervals are plotted for each treatment. Whether a male preferred to construct his first nest with a novel material did not depend on the socio-ecological environment he experienced as a juvenile (preference for novel material versus other material across all treatments: adult access term, χ2 = 0.83, n = 29, P = 0.360; material access term, χ2 = 2.80, n = 29, P = 0.094; adult access×material access term, χ2 = 0.01, n = 29, P = 0.909; Model 3; Figure 2a, right panel). Construction speed The juvenile social and ecological environment together also affected the speed with which zebra finches initiated (adult access × material access term, χ2 = 6.08, n = 28, P = 0.014; Model 4), and completed (adult access×material access term, χ2 = 6.53, n = 28, P = 0.011; Model 5), their first nest. Males without juvenile access to both an adult and material (A−/M− treatment; dashed red lines in Figure 2b) were more than four times slower to make their first material deposit (hazard ratio [HR] = 4.15, lower and upper 95% confidence interval (CI) = 1.38–12.48, n = 28, P = 0.011) and close to three times slower to deposit the remaining material into their nest (HR = 2.72, 95% CI = 1.00–7.40, n = 28, P = 0.049), compared with the males in the other three treatments. These data, taken together, support the hypothesis predicting interactive effects of the juvenile socio-ecological environment on first-time nest-construction speed. Follow-up analyses: potential mechanistic explanations Causal mechanisms underlying early-life social effects are often hard to test (Taborsky 2016). Because we filmed the juvenile early-life environment, however, we were able to examine potential links between juvenile and adult birds’ amount of material handling (defined here as bill-to-material contact) in the material experience sessions, and how the juveniles then went on to construct their first nest (video scoring and statistical details on how we did this are reported in the Supplementary Material). We focused on the material they preferred for and not their speed at first-time nest construction, as our results, reported above, showed that juvenile material access is not essential to shaping first-time nest-construction speed (e.g., males in the A+/M− and M+ treatments were similarly speedy at constructing their first nest; Figure 2b). How might the early social environment bias animals towards a preference for using one particular kind of raw material? Firstly, corvid and primate field data suggest that adults increase youngsters’ engagement with raw material (because youngsters will interact more with raw material/material artifacts in the presence of adults; e.g., Humle et al. 2009; Holzhaider et al. 2010a). Contrary to these field data, however, our juvenile zebra finches with an adult groupmate tended to spend less time in each material experience session handling the material than did the juveniles without an adult groupmate (mean ± SE seconds spent handling material across the 12 material experience sessions: 208.58 ± 21.58 versus 417.11 ± 26.85, respectively; Figure 2c, left panel), although this between-treatment difference in juveniles’ material-handling time remained nonsignificant (adult access × material session term, χ2 = 18.42, n = 167 from the 16 juveniles, P = 0.072; Model 6). Secondly, social learning is considered to play a potent role in the development of animal material technology, as exemplified by the considerable number of studies wherein researchers report on how much time juveniles seem to spend watching adults’ material-use behavior e.g., Ottoni et al. 2005; Humle et al. 2009; Holzhaider et al. 2010a, 2010b; Coelho et al. 2015. Although we do not know, for our birds at least, how much time adults might need to engage with the material before juvenile groupmates prefer to use that material in adulthood, we can rule out one possibility: adults need to engage with material more than juvenile groupmates. In each of the material experience sessions, adults spent markedly less time than their juvenile groupmates handling the material (mean ± SE seconds spent handling material across the 12 material experience sessions: 37.07 ± 5.74 versus 208.58 ± 21.58, respectively; Figure 2c, right panel), a significant within-treatment difference that increased as juveniles gained material-handling experience (age×material session term, χ2 = 29.80, n = 127 from the eight juveniles and four adults, P = 0.002; Model 7). In summary, these data suggest that adult presence, rather than individual or observational experience of raw-material handling, plays a more important role in the development of material preference than has been previously considered. DISCUSSION In the wild, experienced adults likely aid the acquisition of material technology in developing animals by increasing the salience of specific raw material and, thus, the constituent physical properties; this in turn might explain apparent within- or between-species raw-material preference(s) (or technological traditions; Fragaszy 2011; Fragaszy et al. 2013). The current data provide compelling experimental evidence to support this view: they show that material preference in male zebra finches that is based on a physical property (color) is shaped by juvenile experience of this material but only in the presence of an adult. There is more to technological competence, however, than simply the choice of a suitable material—effective execution of the task is key to the adaptive value of skilled behavior (Bateson 1988). Here, too, our study unveils early-life social and ecological drivers of construction ability in male zebra finches: adult presence and access to raw material. Indeed, juvenile social and material impoverishment together led these males, as adults, to be both slower to initiate and complete first-time nest construction, than were males provided with juvenile access to an adult, material, or both. The above results, taken together, show the early-life socio-ecological environment shaped zebra finches’ first-time nest construction, and crucially, reveal that these early-life effects prevailed upon individuals during the juvenile, and not the natal, developmental phase. The juvenile period of development in zebra finches is also critical to their early learning of appropriate mate choice and vocal production. To develop species-typical mate preference and song, recently fledged, juvenile zebra finches require, respectively, exposure to (e.g., Immelmann 1972), or guided feedback from (Carouso-Peck and Goldstein 2019), an adult conspecific before reaching sexual maturity, whereafter both behaviors become fixed. As adult birds will modify their construction behavior based on previous breeding experience (see table 3 in Breen et al. 2016), we do not suppose that such fixation occurs with respect to avian nest construction. But our data reveal hitherto unknown parallels, in terms of timing and environmental cues, between the development of song, mate choice, and nest construction in zebra finches. It seems likely that the juvenile socio-ecological environment plays a more dominant role in the development of animal material technology in general. In the wild, both the amount of individual material-use practice and social material-use guidance (where “guidance” is defined as the opportunity to observe proficient adults, without implying any active process such as teaching) experienced by juveniles are thought to relate to technical skill-competence in later life (Biro et al. 2006; Fragaszy 2011; Fragaszy et al. 2013; Meulman et al. 2013; Breen et al. 2016; Rutz et al. 2018). Our findings that neither the amount of time juveniles spent handling material nor that spent by their adult groupmate appear related to how they construct their first nest, were, thus, fairly surprising. Indeed, juvenile exposure to an adult conspecific seems sufficient experience (Figure 2b) to ensure that speed at first-time nest construction is comparable to that of males that had juvenile material-handling experience. These data imply that juvenile adult access and juvenile raw-material access had similar but nonadditive effects on first-time nest-construction speed. These effects may be buffering or enhancing in nature as, on the one hand, adult presence in early life can safeguard developing builders against later behavioral inefficiency (e.g., prolonged contest resolution over resources; Taborsky et al. 2012), while on the other hand, mandibulation of material in early life can lead to faster nest construction in adulthood (Collias and Collias 1964). In any case, the current study reveals the convergent effect that early-life social and ecological factors can have on the development of technological competence. It is less clear, however, to what extent, if at all, juvenile and/or adult males living together need to handle material in order for developing males to acquire a preference for, or to learn, this stimulus. Variation in behavior can be generated by a multitude (Hoppitt and Laland 2008) of social processes such as social facilitation—a clear candidate for future testing—as well as social factors such as differences in sex, age, and genetic relatedness (Lonsdorf and Bonnie 2010). And we note that our data do not exclude a role for these social dynamics in the development of zebra finches’ nest construction and animal material technology more generally; rather, they both encourage discussion of and invite much-needed (Taborsky 2016) study on candidate causal mechanisms in developmental experiments. It is also worth noting that the experimental approach applied here revealed clear effects of the early-life environment on adult phenotype, despite our modest sample size. For example, the interactive effect of the juvenile social and ecological environment on first-time construction speed—that is, a 4- and nearly 3-fold reduction in the speed at which novice builders in the A−/M− treatment initiated and completed their nest, respectively—was considerable, given that a reduction in speed of a 2.8 magnitude or greater constitutes a large effect size (Azuero 2016). We anticipate that our experimental approach applied to other study systems with shorter (and, therefore, less experimentally time-consuming) developmental periods, coupled with the implementation of automated tracking technology, will facilitate faster collection of larger and richer datasets, from both laboratory and natural environments. Rodents, for example, may be one such study system, as there is tantalizing evidence of early-life socio-ecological effects on nest construction in adults (Van Loo and Baumans 2004; Margulis et al. 2005), and methods available for successful automatic recording of behavior (e.g., social interactions and movement patterns) among individuals living together either in the laboratory (e.g., Freund et al. 2013) or in the wild (e.g., König et al. 2015). As we have shown, this type of approach should illuminate whether, and, if so, when different early-life environmental factors, in isolation or in combination, shape animal material technology. For nest construction in zebra finches, future study could now focus on whether material preference follows a two-stage developmental process—the consolidation or modification of initial preference—akin to that which underpins their choice of mate (Immelmann et al. 1991; Kruijt and Meeuwissen 1991; Kruijt and Meeuwissen 1993). Indeed, as wild zebra finches breed colonially (Zann 1996) and prospect on neighbors’ nests (Brandl et al. 2019), and nests themselves can influence laboratory-bred zebra finches’ material preference (Breen et al. 2019), it seems plausible that they may “double-check” early-life information on material suitability. Alternatively, future study could examine whether variation in nest-construction speed as a consequence of variation in the early-life environment leads to differences in birds’ reproductive success. Females of other bird species appear to lay sooner in response to a perceived increase in material collection effort by their mate (Soler et al. 1996; Soler et al. 2001), and the timing of clutch initiation can have knock-on effects on recruitment in wild bird populations (Verhulst and Tinbergen, 1991; Weggler, 2006). There is much scope for future research. CONCLUSIONS The current study confirms that the early-life socio-ecological environment can drive variation in animal material technology. Phenotypic variation is essential to evolution by natural selection. Understanding advancements in animal material technology, then, demands focus on the early-life environment. Indeed, our finding that both juvenile early-life adult and raw-material access affect novice builders’ material preference and construction speed has important implications for the profitability of construction endeavors—individuals may avoid selecting “bad” (e.g., too conspicuous, Bailey et al. 2015; too long, Muth and Healy 2014; or too flexible, Bailey et al. 2014) material and losing valuable time (Mainwaring and Hartley 2013)—and, thus, for individual survivorship and reproductive success, which likely affects the evolution of animal construction. We suggest that the zebra finch, then, is not only a useful model system for understanding how experience shapes construction behavior (Breen et al. 2016), but also how differences in animal material technology arise and persist. FUNDING This work was supported by funding from the School of Biology and a St Leonard’s College Scholarship at the University of St Andrews, UK (both to A.J.B), as well as the Biotechnology and Biological Sciences Research Council (Anniversary Future Leader Fellowship to L.M.G.; grant number: BBSRC—BB/M013944/1). AUTHORS’ CONTRIBUTIONS A.J.B. and L.M.G. conceptualized and designed the experiment. A.J.B. performed the experiment and extracted the data, with help on video scoring (K.E.L., C.G., and J.C.) and animal husbandry (S.C.E.). A.J.B. analyzed and visually presented the data. A.J.B. wrote the manuscript, which was edited by S.D.H. and L.M.G. and approved by all authors. 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TI - Juvenile socio-ecological environment shapes material technology in nest-building birds
JF - Behavioral Ecology
DO - 10.1093/beheco/araa027
DA - 2004-10-01
UR - https://www.deepdyve.com/lp/oxford-university-press/juvenile-socio-ecological-environment-shapes-material-technology-in-V1AONYKG4x
SP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -