Journal of Comparative Psychology

A Comparison of Spontaneous Problem-Solving Abilities in Three Estrildid Finch (Taeniopygia guttata, Lonchura striata var. domestica, Stagonopleura guttata) Species Martin Schmelz, Oliver Krüger, Josep Call, and E. Tobias Krause Online First Publication, August 24, 2015. http://dx.doi.org/10.1037/a0039646

CITATION Schmelz, M., Krüger, O., Call, J., & Krause, E. T. (2015, August 24). A Comparison of Spontaneous Problem-Solving Abilities in Three Estrildid Finch (Taeniopygia guttata, Lonchura striata var. domestica, Stagonopleura guttata) Species. Journal of Comparative Psychology. Advance online publication. http://dx.doi.org/10.1037/a0039646 Journal of Comparative Psychology © 2015 American Psychological Association 2015, Vol. 129, No. 4, 000 0735-7036/15/$12.00 http://dx.doi.org/10.1037/a0039646

A Comparison of Spontaneous Problem-Solving Abilities in Three Estrildid Finch (Taeniopygia guttata, Lonchura striata var. domestica, Stagonopleura guttata) Species

Martin Schmelz Oliver Krüger Max Planck Institute for Evolutionary Anthropology Bielefeld University

Josep Call E. Tobias Krause Max Planck Institute for Evolutionary Anthropology, and Bielefeld University, and Friedrich-Loeffler-Institut University of St Andrews

Cognition has been extensively studied in primates while other, more distantly related taxa have been neglected for a long time. More recently, there has been an increased interest in avian cognition, with the focus mostly on big-brained species like parrots and corvids. However, the majority of bird species has never systematically been studied in diverse cognitive tasks other than memory and learning tasks, so not much can yet be concluded about the relevant factors for the evolution of cognition. Here we examined 3 species of the estrildid finch family in problem-solving tasks. These granivorous, non-tool-using birds are distributed across 3 continents and are not known for high levels of innovation or spontaneous problem solving in the wild. In this study, our aim was to find such abilities in these species, assess what role domestication might play with a comparison of 4 genetically separated zebra finch strains, and to look for between-species differences between zebra finches, Bengalese finches, and diamond firetails. Furthermore, we established a 3-step spontaneous problem-solving procedure with increasing levels of complexity. Results showed that some estrildid finches were generally capable of spontaneously solving problems of variable complexity to obtain food. We found striking differences in these abilities between species, but not between strains within species, and offer a discussion of potential reasons. Our established methodology can now be applied to a larger number of bird species for phylogenetic comparisons on the behavioral level to get a deeper understanding of the evolution of cognitive abilities.

Keywords: cognition, estrildidae, string test, bar test, lid test, songbird

Supplemental materials: http://dx.doi.org/10.1037/a0039646.supp

How cognition evolved is one of the major outstanding ques- For instance, the “Social Intelligence Hypothesis” posits that spe- tions of contemporary comparative psychology. Over the years, cies living in groups of high social complexity are likely to evolve several hypotheses have been proposed to explain this process. high cognitive skills sustained by larger brains (Byrne & Whiten, Initially, only nonsocial environmental problems such as coping 1988; Dunbar, 1995; Humphrey, 1976). Each of these hypotheses with ephemeral resources in space and time (Milton, 1981) or was developed and tested using data on primates exclusively (e.g., extracting resources embedded in various substrates (Parker & Amici, Aureli, & Call, 2008; Deaner, van Schaik, & Johnson, Gibson, 1977) were considered as the main selection pressures 2006; Dunbar, 1992)—something that made it difficult to actually behind cognitive evolution. More recently, however, hypotheses assess their general predictive value across a broader zoological This document is copyrighted by the American Psychological Association or one of its allied publishers. incorporating some aspect of sociality have also come into focus. scale. Fortunately, nonprimates were later included in analyses This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

Editor’s Note. Charles Snowdon served as action editor for this article. Institute of Animal Welfare and Animal Husbandry, Friedrich-Loeffler- Institut. We thank Edda Geißler for help in preparing the experiments, and we thank Werner Jamin for building some of the experimental apparatuses. We Martin Schmelz, Department of Developmental and Comparative thank Marike Schreiber for help in preparing the figures. We also thank Dr. Psychology, Max Planck Institute for Evolutionary Anthropology; Ol- Charles T. Snowdon and four anonymous reviewers for valuable comments iver Krüger, Department of Animal Behaviour, Bielefeld University; on an earlier version of the manuscript. Josep Call, Department of Developmental and Comparative Psychol- Correspondence concerning this article should be addressed to E. Tobias ogy, Max Planck Institute for Evolutionary Anthropology, and School Krause, Institute of Animal Welfare and Animal Husbandry, Friedrich- of Psychology and Neuroscience, University of St Andrews; E. Tobias Loeffler-Institut, Doernbergstrasse 25/27, 29223 Celle, Germany. E-mail: Krause, Department of Animal Behaviour, Bielefeld University; and [email protected]

1 2 SCHMELZ, KRU¨ GER, CALL, AND KRAUSE

investigating the relation between socioecological factors and var- ences that might be based on their ecology, sociality, phylogeny, ious measures such as brain size or innovation that have been often and geographical distribution among other factors. considered as a proxy for complex and flexible cognition (Dunbar, We suggest that the two most pressing issues of avian cognition 1995; Lefebvre, Whittle, Lascaris, & Finkelstein, 1997). One lim- today are to assemble as much inter- and intraspecific data from as itation of these analyses is that they are based on measures that are many different species as possible and to find and establish simple either too coarse or only measure cognitive function indirectly. but informative methods to test and compare basic cognitive The current interest in cognitive evolution has coincided with abilities. This would combine the rigor of the experimental method (and indeed facilitated) an increased interest in animal cognition in with the power of the comparative method applied to a large general. There has been a concerted effort to investigate various number of species. This approach has been recently used to inves- cognitive abilities in a systematic fashion in several nonprimate tigate inhibitory control in 36 species (MacLean et al., 2014). We groups (for an overview, see Shettleworth, 2010). Numerous ex- propose to use the same basic approach (with some improvements perimental studies have shown remarkable cognitive abilities in as noted below) to investigate spontaneous problem solving, an birds, especially in corvids and parrots, that are sometimes quite ability that allows individuals to extract food that is currently out comparable with primate abilities (Emery, 2006; Emery & Clay- of reach. Individuals capable of getting access to such food re- ton, 2004). Thus, several of these large-brained bird species were sources may possess an advantage over other individuals because shown to be adept tool users (Hunt, 1996; Hunt & Gray, 2004), they can potentially expand the amount and the spectrum of food even if they do not show that behavior in the wild (Chappell, available to them (Overington, Griffin, Sol, & Lefebvre, 2011)— 2006). They are good social learners (Cornell, Marzluff, & Pec- something that is particularly important when food becomes rare oraro, 2011; Templeton, Kamil, & Balda, 1999), used causal or when embedded food is especially valuable. reasoning and inferences in search for food (Schloegl, Schmidt, To test the problem-solving skills of birds in extractive foraging Boeckle, Weiß, & Kotrschal, 2012; Taylor, Hunt, Medina, & Gray, contexts, we developed an instrument composed of three tests used 2009; Taylor, Miller, & Gray, 2012), and flexibly solved problems in previous studies: string (e.g., Seibt & Wickler, 2006), bar (e.g., (Auersperg, von Bayern, Gajdon, Huber, & Kacelnik, 2011; Bird Mateos-Gonzalez, Quesada, & Senar, 2011), and lid (e.g., Fisher & & Emery, 2009; Heinrich & Bugnyar, 2005; Seed, Clayton, & Hinde, 1949). Each of these tasks required subjects to manipulate Emery, 2008). Birds could represent objects outside of their per- parts of an apparatus to gain access to food. Our instrument ception (“object permanence”; Pepperberg & Funk, 1990; Pollok, possessed three crucial features. First, the three tasks differed in Prior, & Güntürkün, 2000; Ujfalussy, Miklósi, & Bugnyar, 2013) their presumed degree of difficulty with the string and the lid being and showed flexible impulse inhibition of food consumption (Au- the easiest and the hardest tasks, respectively. This is important ersperg, Laumer, & Bugnyar, 2013; Dufour, Wascher, Braun, because it allowed us to better capture within- and between-species Miller, & Bugnyar, 2012). Different studies even suggest some variability and also to analyze each task either separately or “theory of mind” abilities in corvids (Bugnyar & Heinrich, 2005, together as a composite score. Second, each of the tasks required 2006; Bugnyar & Kotrschal, 2004; Clayton, Dally, & Emery, only basic manipulations on the subject’s part (e.g., pulling, de- 2007; Thom & Clayton, 2013). The focus of these studies was taching, or removing parts of the apparatus), and no training was mostly on species with relatively big brains like parrots and necessary prior to the test. Problem solving therefore had to occur especially corvids (e.g., Iwaniuk, Dean, & Nelson, 2005). Cogni- tive abilities of other bird species, like pigeons and several others, spontaneously during the task. Third, the instrument was easy to have been studied experimentally mostly with regard to their administer, and the apparatuses easy to build. Taken together, this spatial memory and associative learning skills (e.g., Biegler, means that a large number of individuals/species could be poten- McGregor, Krebs, & Healy, 2001; Dawkins, Guilford, Braith- tially tested in a relatively short period of time. Presenting them waite, & Krebs, 1996; Greenberg, 1985; Klopfer, 1959; Krebs, with identical, simple, and relevant problems—the access to food Healy, & Shettleworth, 1990; Shettleworth & Krebs, 1982). is blocked—is a useful starting point for controlled comparisons of A general assumption is that corvids and parrots might be a variety of species, even though the specific manipulations nec- special within birds in a similar way that primates are supposed to essary to solve the tasks might always be more or less appropriate be cognitively special within mammals (Emery, 2006). In fact, it for specific species. has been argued that parrots and corvids, just like primates, pos- We administered our instrument to zebra finches (Taeniopygia This document is copyrighted by the American Psychological Association or one of its allied publishers. sess complex social lives made possible by large brains (Emery & guttata) and two closely related species, Bengalese finches (Lon- This article is intended solely for the personal use of the individual user and is not to be disseminated broadly. Clayton, 2004; Seed, Emery, & Clayton, 2009). Paradoxically, the chura striata var. domestica) and diamond firetails (Stagonopleura current emphasis on corvids and parrots has recreated the original guttata). Zebra finches are one of the most intensively studied bird problem of exclusively concentrating on a handful of species species in behavioral sciences (Griffith & Buchanan, 2010; Zann, belonging to the same zoological group. If a few decades ago 1996). They are songbirds that belong to the monophyletic family cognitive theories were based and tested on primates, now they of the Estrildidae (Arnaiz-Villena et al., 2009; Christidis & Boles, have been transformed into theories concentrating on primates, 2008) as do the other species in the current study. Nowadays, there corvids, and parrots. Most bird species have never systematically are many different strains of zebra finches available, with pheno- been studied in diverse cognitive tasks other than learning and typic differences due to human domestication and breeding effort memory studies (Emery, 2006), so absolute statements about cog- (Forstmeier, Segelbacher, Mueller, & Kempenaers, 2007; Hoff- nitively special bird families and the general reasons for their man, Krause, Lehmann, & Krüger, 2014; Zann, 1996). Two ex- specialization remain untested. Much more research is needed to amples are white zebra finches and the black cheek zebra finches, fill the void and obtain a clearer picture of cognitive abilities in all which are both part of this study (see methods for details). Sur- birds to then be able to look for systematic similarities and differ- prisingly, even in this common study animal, cognitive tasks have PROBLEM-SOLVING IN ESTRILDID FINCHES 3

been largely neglected (Brust, Krüger, Naguib, & Krause, 2014; home cage (83 ϫ 30 cm and 40 cm high), the birds were kept in Healy, Haggis, & Clayton, 2010; Larose & Dubois, 2011). mixed-sex groups of 4 (2:2) with respect to their strain and had ad We judged zebra finches, and estrildid finches in general, to be libitum access to water and food, that is, seed mix (provided on the an excellent starting point to broaden the picture of bird cognition ground) and millet (provided on an elevated perch). Twelve adult for four main reasons. First, granivorous estrildid finches are not animals (6 of each sex) of both the BF (details of the stock, see known for their high levels of innovation and spontaneous problem Krause & Caspers, 2012) and the DF (details of this stock, see solving in the wild (Healy et al., 2010; Overington, Morand- Krause et al., 2014) were tested and housed in the same way as the Ferron, Boogert, & Lefebvre, 2009). Basic problem-solving abil- different ZF strains. Thus, in total, 72 birds from the three species ities in estrildid finches would therefore be especially interesting were tested. All subjects had no prior experience with the tests or as it would suggest these abilities are present even in species that with testing procedures that involved object manipulation in order do not seem to display them in their natural environment. Second, to obtain food or with any learning or cognitive tests. They had estrildid finches are a particularly interesting bird family for such been moved to the room where the tasks were conducted 2 weeks studies as the species are distributed across three continents (Af- prior to the experiment but had no visual access or habituation to rica, Asia, Australia) and thus experience massive ecological vari- the test cages or test apparatuses during this time. All subjects were ation. Third, their phylogeny is quite well established (Arnaiz- used to feeding on the ground and on elevated locations and also Villena et al., 2009). Fourth, there are multiple strains of a same to being handled (for taking biometric measures) and being trans- species available in captivity. This offers the unique opportunity to ferred between different cages. investigate the effect of domestication and differential artificial All birds were tested on 3 different days in three tasks. They all breeding on cognition. received them in the same order: first the “string test,” then the The challenge of assessing problem-solving skills in estrildid “bar test,” and finally the “lid test” (see below for details). Birds finches and, more generally, developing the tools to make mean- were food- and water-deprived for 4–4.5 hr and were subse- ingful comparisons within and between species is the overall goal quently tested for 30 min. They were captured by the experimenter of the current study. More specifically, we aim at: (a) establishing from their home cage and immediately transferred to the test cage. a three-step spontaneous problem-solving instrument for non-tool- During these 30 min, no experimenters were present in the room using estrildid finches with increasing levels of complexity, (b) while the birds were videotaped. They were separated from con- assessing if there are cognitive within-species differences in four specifics visually but not acoustically or olfactorily. genetically separated zebra finch strains (with possible relations to Tasks were conducted in a big test cage (80 cm ϫ 50 cm ϫ 60 their domestication), and (c) finding between-species differences cm), with the experimental apparatuses being placed on the left between species of estrildid finches that are native to different and right side of the floor symmetrically. After the birds finished ecological and social environments, two of them sympatric in the test, they were released back into their home cages with water Australia, the third one a domesticated form of an Asian species. and food ad libitum.

Method Materials and Procedures

Subjects In the following three tests, the birds were always presented with two options: a functional/baited option in which food could In the following experiment, three estrildid finch species were be successfully retrieved and a nonfunctional/unbaited option in tested: zebra finches (Taeniopygia guttata; abbreviated in the which food was either unreachable or not present. We introduced following as ZF), Bengalese finches (Lonchura striata var. domes- these options in order to assess if birds simply manipulated any tica; BF), and diamond firetails (Stagonopleura guttata; DF). We apparatus present randomly or if their behavior was targeted on the used four strains of ZF to examine whether domestication might functional/baited option to retrieve the food. have affected their behavior. Three strains can be separated using String test. The goal in the string test was to pull a string that molecular markers (Forstmeier et al., 2007; Hoffman et al., 2014): was attached to food (a piece of millet, ca. 5 cm long) in order to (a) The “domesticated zebra finches” (referred to as “Bielefeld” in access it. There were two transparent Perspex tubes (18 cm long, Forstmeier et al., 2007), which cluster with the European domes- 5 cm diameter) in the test cage that were closed on one side and This document is copyrighted by the American Psychological Association or one of its allied publishers. ticated strains. (b) “Australian zebra finches,” which originated half-open on the other side so that the birds could not enter the This article is intended solely for the personal use of the individual user and is not to be disseminated broadly. from wild Australian birds, have been bred in captivity for a few tubes to reach the food. In one of the tubes (side randomized and generations only (referred to as “Bielefeld-AUS” in Forstmeier et counterbalanced among sex and strain/species), there was a piece al., 2007) and cluster with the wild Australian birds. (c) “White of foxtail millet that was attached to a string (ca. 14 cm long); in zebra finches” (referred to as “Bielefeld-white” in Forstmeier et the other tube, an identical piece of food and string were present, al., 2007), which have a white phenotype, lack male ornament but they were not connected with a gap of ca. 2 cm between food (except beak color intensity), and also cluster with the European and string. Approximately 7 cm of both strings stuck out of the domestic birds. The fourth strain—“black cheek zebra finches” (in respective tubes (see Figure 1a). This means that one piece of food the following referred to as “black zebra finches”)—was only could be pulled out with the string, while the other one was recently established at Bielefeld University, and molecular data inaccessible and pulling on the string had no effect. has not been published yet. However, this strain seems genetically Bar test. The goal in the bar test was to remove wire bars from not to cluster with any of the three mentioned above (Hoffman, the top of a container to access food (seed mix) inside. There were Krüger, Krause, unpublished data). From each of the four zebra two transparent glass containers (7.5 cm ϫ 7.5 cm ϫ 3 cm) in the finch strains, 12 adult birds were tested (6 of each sex). In their test cage that were open on the top side, one containing food on the 4 SCHMELZ, KRU¨ GER, CALL, AND KRAUSE

cm) for birds to access the aluminum foil lids, and if the lid was removed, to feed from the seed mix in the baited glass container. To reach the food, the aluminum foil lid had to be either lifted and removed or pecked through. We chose these three tests because we reasoned that they constituted a graded series of increasing cognitive difficulty. We designed the string test to be the easiest, as in the string test the solution (i.e., the string) to get the reward was directly connected to the reward (food), and the food reward was directly visible. The intermediate test was the bar test as the food was visible when manipulating and removing the solution (i.e., a wire bar), but it was not directly connected to the reward. The most difficult test was the lid test, as the solution (i.e., the lid) was opaque, and the food was not visible from the platform during the manipulation. Thus, when solving this task, the animals could not see an imme- diate connection between reward and solution. However, our as- sumptions about the increasing level of difficulty had to ultimately be confirmed by the results.

Measures Problem solving. We measured whether an individual had solved the problem, that is, pulled out the rewarded string in the string test, pulled out a bar from the rewarded side in the bar test, or opened the lid from the rewarded glass in the lid test, to get access to the food source as a binomial “0” (no success) or “1” (success) score (e.g., videos for each task see the online supple- mentary material S2–S4). Average latencies of the successful birds until they solved the task, number of unsuccessful manipulations prior to success, and whether they manipulated the baited or the Figure 1. Schematic figure of the rewarded sites of the experimental apparatuses: the string test (a), the bar test (b), and the lid test (c). control apparatus first are shown in the online supplemental ma- Additional photos of the three experimental apparatuses are provided in the terial S1. online supplemental material (Figure S1a–c). Activity scores/neophobia. In addition to the measure whether individuals solved the problem, we measured the ap- proach of the birds to the rewarded and the control side of each test ground (ca. 0.5 cm high) and one being empty. Two small pieces apparatus using activity scores as a proxy for the gradient from of cardboard paper with 11 holes (at ca. 0.6 cm intervals) were neophobia/avoidance to boldness/exploration toward the appara- attached on two sides of both containers. Through these holes, 11 tuses. These scores were measured from the videos using the pieces of metal wire (ca. 13.5 cm long and 1 mm thick) were following scoring system: (0) no approach to the vicinity of the pushed so that ca. 3 cm of these wire bars protruded on each side experimental apparatus. Vicinity is defined as the area of one body of the containers (see Figure 1b). The gaps between the bars were length around the apparatus; (1) approach to the vicinity of the too small for the birds to feed through them. In order to reach the experimental apparatus but no contact; (2) contact to any part of food in the baited container, at least one wire bar had to be the experimental apparatus, except to the “solution” of the respec- removed sideways through the paper holes. If one bar was re- tive problem (i.e., string/bar/lid); (3) contact to/manipulating/mov- This document is copyrighted by the American Psychological Association or one of its allied publishers. moved, the gap of approximately 1.2 cm was sufficient for the ing the “solution” with any part of the body except the beak; (4) This article is intended solely for the personal use of the individual user and is not to be disseminated broadly. birds to reach the food. contact to/manipulating/moving the “solution” with the beak, Lid test. The goal in the lid test was to remove a lid made of which we assumed to be the only body part with which the aluminum foil from a glass container to access food (seed mix) problems could be solved. Thus, a low-activity score generally inside. There were two transparent glass containers (conventional indicated a higher level of neophobia, whereas a high-activity drinking glasses, 13.5 cm high, 5.5 cm diameter on bottom and 6.0 score generally indicated a higher level of exploration and engage- cm diameter on top), one filled with seed mix up to approximately ment with the apparatus. 1 cm below the top and the other one being empty. Both containers The videos were analyzed and scored by one observer, who were closed with a round piece of aluminum foil (about 7.3-cm scored both the control and the rewarded side for all 216 videos. A diameter) that was folded around the rims of the containers (see second observer analyzed Ͼ20% of randomly selected videos of Figure 1c; photographs of the three experimental apparatuses are each of the three tests, that is, 44 videos in total. Interobserver also provided in the online supplemental material, Figure S1a–c). reliability was tested using Cohen’s ␬ (Cohen, 1968). The second Between the two containers, there was a sitting platform (12 cm ϫ observer agreed with the behavior scores of the first one at a very 15 cm) in the middle of the test cage at the right height (about 12.5 high rate (88.6% of scores; Cohen’s ␬ϭ0.86). PROBLEM-SOLVING IN ESTRILDID FINCHES 5

Statistical Analysis The success in problem solving was analyzed for the within- species comparison of the zebra finch strains using a Fisher’s exact test (2 ϫ 4 matrix; i.e., 2 ϭ solvers/nonsolvers ϫ 4 ϭ number of strains). No within-species differences between the four zebra finch strains were found, so we pooled them for the between- species comparisons (details see below, all p Ͼ .60). Between- species comparison of the problem solving success of the three estrildid finch species was done with Fisher’s exact test (2 ϫ 3 matrix). When this test was significant, pairwise post hoc compar- isons were conducted with a Fisher’s exact test (2 ϫ 2 matrix). We used a Friedman test to compare the success across the three problem-solving tasks. The scores (in the problem-solving analysis and activity scor- ing) between rewarded and control side were compared by calcu- lating the difference (score rewarded side minus score unrewarded side), and testing this value using one-sample t tests against an expected value of zero. For species and strain comparison of the activity scores at the rewarded side, Kruskal-Wallis (KW) analysis of variance (ANOVA) was used. In case of a significant KW ANOVA, a post hoc comparison after Siegel and Castellan (1988) for pairwise comparisons was used. All statistical tests were cal- culated two-tailed using R 2.15.2 and Statistical Package for the Social Sciences (SPSS) 20.

Ethical Note The experiments were carried out according to the German Laws for experimentation with animals. Housing of the birds was conducted under permission of the Veterinäramt Bielefeld, Ger- many (#530.4, 24.07.2014). After the end of the study, all birds remained in the lab stock at Bielefeld University.

Results

Within-Species Comparisons of the Four Zebra Finch Strains The four strains of zebra finches (domesticated ZF, Australian ZF, white ZF, and black ZF) did not differ in their problem-solving abilities in any of the three tasks, all p Ͼ .60. In total, 12 (3 domesticated ZF; 3 Australian ZF; 2 white ZF; and 4 black ZF) out Figure 2. Number of successful (dark gray bars) and unsuccessful (light gray bars) individuals of the three estrildid species (four zebra finch strains, of the 48 ZF (25%) solved the string test, that is, pulled out the ZF; Bengalese finch, BF; diamond firetail, DF) in the three problem baited string. There was no difference in their success rate among This document is copyrighted by the American Psychological Association or one of its allied publishers. solving tasks: string test (a), bar test (b), and lid test (c). the four strains, Fisher’s exact test, p ϭ .97. Three ZF out of 48 This article is intended solely for the personal use of the individual user and is not to be disseminated broadly. (6.25%) solved the bar test, that is, removed a bar on the baited side (2 Australian ZF and 1 black ZF). There was no difference in species (ZF, BF, DF) differed significantly in their success in their success rate among the four strains, Fisher’s exact test, p ϭ spontaneously solving the string test (Fisher’s exact test, p ϭ .005; .60. No ZF solved the lid test, that is, removed the lid on the baited Figure 2a). Post hoc pairwise comparisons of species revealed that side and thus there was no difference among the four strains. DF were significantly more successful than BF, p ϭ .005, and also more successful than ZF, p ϭ .039. ZF and BF did not differ Between-Species Comparison significantly in their success rate, but there was a trend of ZF being more successful, p Ͻ .10. We found significant differences in the problem-solving abili- ZF (see above) and DF individuals solved the bar test. Five out ties among the three estrildid finch species ZF, BF, and DF in the of 12 DF solved the bar test (i.e., 41.7%), while none of the BF was string test and in the bar test. ZF (see above) and DF individuals successful. The three species (ZF, BF, DF) differed significantly in solved the string test. Seven out of 12 DF solved the string test their success in solving the bar test, Fisher’s exact test, p ϭ .006 (i.e., 58.3%), while none of the BF was successful. The three (Figure 2b). Post hoc pairwise comparisons revealed that DF were 6 SCHMELZ, KRU¨ GER, CALL, AND KRAUSE

significantly more successful than BF, p ϭ .037, and were more scores than BF (post hoc comparison string test and bar test p Ͻ successful than ZF, p ϭ .006. The difference between ZF and BF .05; lid test p Ͻ .1). DF and ZF did not differ in their activity in solving the task was not significant, p ϭ 1. scores to the rewarded side in any of the three tests, all post hoc One single DF solved the lid test (8.3%), while none of the ZF comparisons, p Ͼ .1. or any of the BF was successful. However, the success rate among As ZF and DF did not differ in their exploration of the rewarded the three species (ZF, BF, DF) in solving the lid test was not side, they were thus analyzed conjointly when testing whether significantly different, Fisher’s exact, p ϭ .33 (Figure 2c). Note activity on the rewarded and the unrewarded side differed. No that the success rate of all species was relatively low while still difference in the activity scores between rewarded and unrewarded revealing interspecific differences. side in the string test was found (mean difference 0.05 Ϯ 0.14 SE, ϭ ϭ t59 0.36, p .72). However, activity scores to the rewarded site Individual Problem-Solving Abilities Across were significantly higher in the bar and the lid test (bar test: mean Ϯ ϭ ϭ the Three Tests difference 0.82 0.21 SE, t59 3.93, p .0002; lid test: mean Ϯ ϭ Ͻ difference 0.85 0.17 SE, t59 5.12, p .0001). In ZF, a total of 13 individuals solved at least one of the three The BF did not show a difference in activity scores to the tasks (Table 1a). Two of those solved two tests (string and bar). In rewarded and control side compared with zero in all three tests and DF, 7 birds solved at least one of the three tests, but every showed a general low level of activity (string test: mean differ- individual that solved either the bar or lid test had also solved the Ϫ Ϯ ϭϪ ϭ ence 0.08 0.08 SE, t11 1.00, p .34; lid test: mean previous test (Table 1b). Ϯ ϭ ϭ difference 0.58 0.36 SE, t11 1.63, p .13; bar test, one Furthermore, the overall relative success of all subjects in the sample t test could not be calculated as the mean and standard tests decreased significantly with our proposed increasing degree deviation were zero). of difficulty. Nineteen of 72 subjects solved the string test, 8 out of 72 subjects the bar test, and 1 out of 72 subjects the lid test, Friedman Test, ␹2 ϭ 26.0, df ϭ 2, p Ͻ .0001. Discussion We demonstrated that at least some individuals of seed eating, Activity Scores non-tool-using estrildid finches that are not known for high levels of innovation or problem solving were capable of solving different The four strains of ZF did not differ in their activity scores to the problems of variable complexity spontaneously to obtain food. As rewarded side in all three tests, all KW test, all ␹2 Ͻ 4.22, df ϭ 3, far as we know, this is the first time that this has been shown for all p Ͼ .24. The activity scores on the rewarded side in all three zebra finches, a species that has been tested extensively in the lab tests differed significantly among the three species, KW tests, in numerous contexts. Additionally, our instrument, based on a string test: ␹2 ϭ 20.49, df ϭ 2, p Ͻ .0001; bar test: ␹2 ϭ 24.71, series of three tasks, which we assumed to reflect increasing df ϭ 2, p Ͻ .0001; lid test, ␹2 ϭ 11.58, df ϭ 2, p ϭ .003; median complexity, was successful in finding variance between tasks and activity scores to rewarded side (string test/bar test/lid test): ZF between species, but not between different strains within a species. 3.0/4.0/2.0; BF 0.0/0.0/0.0; DF 4.0/4.0/2.0. The post hoc compar- Our assumption of a series of tasks of increasing difficulty was isons for the KW test revealed that in all three tests, ZF had confirmed by our data. significantly higher activity scores than BF (all three post hoc Our results show that some individuals of both Australian es- comparisons: p Ͻ .05). In line with this, DF had higher activity trildid finch species, that is, zebra finches and diamond firetails, had spontaneous abilities of solving problems to obtain food. There were successful zebra finches in two tasks (string test and Table 1 bar test) and successful diamond firetails in all three tasks (how- Overview of the Successful Spontaneous Problem-Solving ever, only 1 individual solved the lid test). On the other hand, no Individuals and How They Behaved Across the Three Tasks individual of the Asian estrildid finch species, the Bengalese finch, Zebra finches Diamond firetails was able to spontaneously solve any of the three tasks. The success (a) (b) rate between the three species differed significantly in the # Sex String Bar Lid# Sex String Bar Lid problem-solving tests. The striking difference between zebra This document is copyrighted by the American Psychological Association or one of its allied publishers. finches and Bengalese finches is especially surprising because

This article is intended solely for the personal use of the individual1 user and is not to Male be disseminated broadly. 1 0 0 1 Female 1 1 0 2 Male 1 0 0 2 Male 1 0 0 both species are often used for cross-fostering in lab studies (e.g., 3 Male 1 0 0 3 Male 1 1 0 Clayton, 1987; Zann, 1985) and have been shown to behave 4 Male 1 0 0 4 Female 1 0 0 similarly in other behavioral situations (e.g., Krause & Caspers, 5 Female 1 0 0 5 Female 1 1 1 6 Female 1 1 0 6 Female 1 1 0 2012). However, not much effort has been devoted to test the 7 Male 1 0 0 7 Male 1 1 0 cognitive abilities of Bengalese finches in those studies. 8 Female 1 0 0 One important aspect to consider when interpreting our results is 9 Male 0 1 0 the interspecific differences in activity level and engagement with 10 Female 1 0 0 11 Female 1 0 0 the apparatuses, which could possibly indicate different levels of 12 Male 1 0 0 neophobia or potentially of persistence. The activity scores of 13 Male 1 1 0 zebra finches and diamond firetails were at similar levels across all Note. In total, 20 different animals of 72 of all three species solved one tests, but the problem-solving success rate differed significantly. or more of the three tasks. The score “1” indicates that the respective bird Thus it seems that at least for these two species, problem-solving solved the task, whereas a “0” indicates that it did not solve the task. abilities did not result from difference in exploration or neophobia. PROBLEM-SOLVING IN ESTRILDID FINCHES 7

In contrast, Bengalese finches hardly explored the test apparatus at rewarded and the control side in the string test. The rewarded and all. The most straightforward interpretation of this finding is that it control side in the string test therefore looked very similar super- might just reflect a high level of neophobia, as indicated by the ficially (the only difference being the attached/unattached string), general low activity scores in this species. Whether this neophobia whereas there was a clear optical difference between rewarded and prevented them from solving the problems in these tasks or control side in the other two tests (baited vs. empty container). whether they were not able to solve these problems at all, needs to Apparently, the optical difference was an important first cue for be explored in future studies. To our knowledge, no differences in which side to explore and therefore helpful in the problem-solving neophobia between zebra finches and Bengalese finches have been process. reported in earlier studies and cross-fostering experiments. Inci- A closer look at the success rates of all birds combined reveals dentally, the massive interspecific differences in the activity scores that success in solving the three different tasks was in agreement highlight the importance of recording these measures in addition to with our assumed level of difficulty: the string test was solved by the measure of success in problem solving. Without the activity 26.4% of all birds, the bar test by 11.1% of all birds while the lid scores, the interpretation of the Bengalese finch performance test was only solved by 1 single individual (1.4% of all birds). It might have been substantially different and might have resulted in is notable that all birds received the three tasks in the same order a potentially false negative interpretation of their problem-solving so that they had no experience of the test situation in the string test abilities. but had already experienced two prior tasks when they were faced To further specify the presence of neophobia and exploration with the lid test. This confirms our proposed increasing levels of differences (which are also likely to exist within species) and its difficulty even more as we might have expected an improvement influence on success, some ideas for future studies might be to (a) over time if the difficulty of all tasks would have been similar or introduce a habituation phase for the birds in the test cage or to test the same. This is an important result because in our opinion test, them in their home cages to reduce stress, (b) investigate the batteries or smaller test series like the one we present here rely on subjects’ propensity to explore novel objects by introducing an variation in difficulty in order to avoid only ceiling or floor effects unknown object into the cage without food present, and (c) inves- that make comparisons impossible—a problem that is also high- tigate the subjects’ propensity to feed out of food containers of the lighted by the complete lack of problem solvers in the Bengalese three tasks when the food is freely accessible. finches in this study, which is difficult to interpret. We also found The finding that activity scores of zebra finches and diamond that individual behavior and success in problem solving were not firetails were higher to the rewarded side than to the unrewarded randomly distributed; individuals that solved one of the more side in both bar and lid test indicate that their problem solving was difficult tasks, in most cases also solved the easier string test not just random exploration. Recall that food was only present on before (Table 1). Thus, it seems that there is individual variation in the rewarded side in the bar test and the lid test, but on both the the ability to solve problems (Seibt & Wickler, 2006).

Table 2 Comparison of the Three Species in Selected Traits of Their Ecology, Lifestyle, and Morphology

Zebra finch Bengalese finch Diamond firetail References

String test solved (at least 1 individual) Yes No Yes This study Bar test solved (at least 1 individual) Yes No Yes This study Lid test solved (at least 1 individual) No No Yes This study Origin Australia Asia Australia Goodwin (1982) Sociality Social Social Less social Immelmann (1965); Robiller (1979) Flock size nonbreeding 150–350 individuals 100 individuals 20–30 individuals Restall (1997); Robiller (1979);

This document is copyrighted by the American Psychological Association or one of its allied publishers. Zann (1996)

This article is intended solely for the personal use ofBreeding the individual user and is not to be disseminated broadly. colony size 50 pairs Large cohesive colonies Up to 12 pairs Birke (1974); Nicolai (2001); Zann (1996) Courtship Song ϩ movement Song ϩ movement Song ϩ movement ϩ grass Nicolai (2001); Zann (1996) stem in the beak Nest material Grass stems ϩ small twigs Grass stems Grass stems Nicolai (2001); Robiller (1979); Zann (1996) Clutch size 4–6 3–6 5–6 Nicolai (2001); Robiller (1979) Diet Grass seeds (eaten from the Grass seeds (eaten from Grass seeds (only eaten from Avery (1980); Immelmann (1965); ground and sometimes the ground), rice, the ground), rarely insects Nicolai (2001); Robiller (1979) from the spike), rarely algae insects (Goodwin (1982); Zann (1996 (ء)Plumage dimorphism Yes No No Climate zone Temperate-subtropical- Tropical Temperate Goodwin (1982); Immelmann tropical (1965); Zann (1996) ,but see Crowhurst, Zanollo (ء) .(Note. For the Bengalese finch, we referred to their wild ancestor species, the white-rumped Munia (Lonchura striata Griggio, Robertson, and Kleindorfer (2012) (mild differences in flanke dots between sexes). 8 SCHMELZ, KRU¨ GER, CALL, AND KRAUSE

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