University of Southern Denmark Behavioural Responses Of

University of Southern Denmark

Behavioural responses of humpback whales to food-related chemical stimuli

Bouchard, Bertrand; Barnagaud, Jean-Yves; Poupard, Marion; Glotin, Hervé; Gauffier, Pauline; Torres Ortiz, Sara; Lisney, Thomas J.; Campagna, Sylvie; Rasmussen, Marianne; Célérier, Aurélie

Published in: P L o S One

DOI: 10.1371/journal.pone.0212515

Publication date: 2019

Document version: Final published version

Document license: CC BY

Citation for pulished version (APA): Bouchard, B., Barnagaud, J-Y., Poupard, M., Glotin, H., Gauffier, P., Torres Ortiz, S., Lisney, T. J., Campagna, S., Rasmussen, M., & Célérier, A. (2019). Behavioural responses of humpback whales to food-related chemical stimuli. P L o S One, 14(2), [e0212515]. https://doi.org/10.1371/journal.pone.0212515

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Download date: 26. Sep. 2021 Behaviour (2019) DOI:10.1163/1568539X-00003539 brill.com/beh

Problem solving capabilities of peach-fronted conures (Eupsittula aurea) studied with the string-pulling test

Sara Torres Ortiz a,∗, Alyssa Maxwell a, Anastasia Krasheninnikova b,c, Magnus Wahlberg a and Ole Næsbye Larsen a a Department of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark b Max-Planck-Institute for Ornithology, Eberhard-Gwinner-Str., DE-82319 Seewiesen, Germany c Max-Planck Comparative Cognition Research Station, ES-Loro Parque Fundación, 38400 Puerto de la Cruz, Tenerife, Spain *Corresponding author’s e-mail address: [email protected]

Received 21 May 2018; initial decision 26 August 2018; revised 25 December 2018; accepted 3 January 2019

Abstract The problem-solving capabilities of four small parrots (peach-fronted conures, Eupsittula aurea) were investigated using string-pulling tests. In seven different tasks, one string was baited following a randomized order. The parrots could retrieve the food reward after a wrong choice as the choice was not forced. Additionally, we applied a non-intuitive pulley task with the strings arranged in front of, instead of below the birds. All four parrots performed very well in the multiple, slanted, and broken string tasks, but all failed in the crossed-string task. Only two parrots solved the single pulley task. All four parrots performed successfully in the multiple pulley task but all failed in the broken pulley condition. Our results suggest that peach-fronted conures solve string-pulling tasks without relying on simple proximity based rules, but that they have evolved cognitive abilities enabling goal-directedness, the understanding of functionality, and a concept of connectedness between two objects.

Keywords cognition, means-end understanding, pulley, parrots.

1. Introduction

String-pulling is one of the most widely used tests in animal cognition because of its easy application and its potential to be applied to different taxa.

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In the past decades, the string-pulling task and its numerous variations have been used in many species of primates, other mammals, and birds (Jacobs & Osvath, 2015). In birds, the paradigm usually involves obtaining a vis- ible, out-of-reach food reward by pulling a vertical string below the bird. Successful string-pulling not only requires sophisticated beak-foot coordination but also sequential production of actions that are not immediately rewarded (Heinrich, 1995). String-pulling has been used to evaluate animals’ understanding of causal relationships and physical continuity, but also their associative learning and the role of using simple rules (Heinrich, 1995; Hein- rich, 2000; DeYoung et al., 2008). Recently, researchers have pointed out that positive perceptual-motor feedback may serve as reinforcement in itself and may therefore play an important role for completing the task (Taylor et al., 2012; Seed & Boogert, 2013). Three important cognitive skills may be elucidated by the string-pulling test: an understanding of means-end relations, functionality, and connectedness. Means-end understanding is expressed as goal-directed behaviour, i.e., the deliberate, planned execution of a sequence of steps to achieve a goal. An obstacle must be overcome to reach that goal, in this case being the distance between the animal and the bait (Piaget et al., 1952; Huber & Gajdon, 2006). However, pulling a string is not always related to functionality, deﬁned as the understanding of the string as a means to reach the food reward. Sometimes animals pull empty strings because the behaviour is self-rewarding (Schuck- Paim et al., 2008). To test whether the animal acts goal-directed or not, the ‘multiple strings task’ may be used, where several vertically hanging strings are presented but only one is attached to a food reward (Figure 1). If the animal chooses the baited string repeatedly, it may be assumed that it is pulling the string in a goal-directed manner. To test the understanding of functionality, the ‘slanted and crossed string tasks’ can be used. Here, the animals are presented with two strings, slanted to one side for the slanted condition, or crossed in the middle for the crossed condition (Figure 1). Only one string is baited, but the bait is positioned directly below and closest to the attachment end of the string that should not be pulled (Figure 1). To solve this task, the subject should either follow the strings visually or, in those cases where the strings are of different colours, associate the colour of the string at the reward end with the colour of the string at the reachable attachment end. Animals can be goal-directed but fail on this so-called proximity error, which means that the subject’s choice is

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek S. Torres Ortiz et al. / Behaviour (2019) 3 based on picking the string attachment end closest to the reward instead of understanding the strings’ configuration. When two rewards are present but only one is in contact with the strings (the so-called ‘broken string task’; Figure 1), the animals need to understand the concept of connectedness to solve this configuration. Animals with means-end understanding do not necessarily understand the concept of connection. They can see that the string is a means to reach the bait without an appreciation of the underlying mechanism. With the broken string condition, it is possible to clarify the existence of this cognitive skill. Although there is a large number of string-pulling studies on birds, most tested subjects belong to only a few families (Jacobs & Osvath, 2015). Most of the species investigated are large-brained species such as parrots and corvids, although recently there has been a study showing positive results for Passeroidea (Audet et al., 2016). Peach-fronted conures are included in the group of Neotropical parrots (Psittaciformes: Psittacidae: Arini; Tavares et al., 2006). Geographically, this group is distributed from Mexico to the extreme south of South America (Forshaw & Cooper, 1989). It is the largest group within the order of Psittaciformes with 30 different genera and 149 of the total of 330 recognized species (Collar, 1997). Among large Neotrop- ical parrots, five species have been tested with the string-pulling paradigm (Schuck-Paim et al., 2008; Krasheninnikova et al., 2013; Krasheninnikova & Schneider, 2014). Hyacinth macaws (Anodorhynchus hiacynthinus; N = 4), Lear’s macaws (Anodorhynchus leari; N = 4), and blue fronted amazons (Amazona aestiva; N = 2) were tested with multiple strings (two strings in this case), crossed strings, and the broken string task. The two species of macaw passed all tasks except the crossed strings condition, and the amazons failed both the crossed strings and the broken string conditions. A fourth species, the orange winged amazon (Amazona amazonica; N = 8), was tested with multiple strings (two strings in this case), crossed strings, and the so-called ‘long string task’ (Figure 1). This parrot species passed the multiple string task but failed the crossed strings and long string configurations. Finally, the fifth species, the green-winged macaw (Ara chloropterus; N = 4) was tested on multiple strings (two strings in this case), crossed strings, broken string, and the long string task. They also failed the crossed string and broken string configuration but passed the long string task. Only one species of smaller sized neotropical parrots has been tested with the string-pulling test. The spectacled parrotlet (Forpus conspicillatus;

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N = 8) passed all the string-pulling tests: multiple strings, slanted strings, crossed strings, and broken string conditions (Krasheninnikova & Wanker, 2010; Krasheninnikova et al., 2013). This performance suggests that this species possesses goal-directed behaviour measured by their understanding that the string can be used to reach an attached food reward (Krasheninnikova et al., 2013). They are also capable of understanding the strings’ configuration (even when these are crossed in the middle and have the same colour) and the concept of connectedness described previously. So, this smaller sized parrotlet shows a better performance than any other Neotropical parrots or Australian and New Zealand parrots, such as the sulphur crested cockatoo (Cacatua galerita; Krasheninnikova et al., 2013) and the kea (Nestor notabilis; Werdenich & Huber, 2006). Previous work has related string-pulling performance to factors such as sociality, foraging behaviour, or beak-foot coordination activities (Magat & Brown, 2009; Krasheninnikova, 2013). However, the possible link between string-pulling behaviour and socio-ecological aspects of the species’ environment remains ambiguous. Little is known about the cognitive abilities of smaller parrots, such as conures (small neotropical parrots of the Aratinga and Eupsittula genus). These parrots usually live in complex fission-fusion societies like those observed in apes (Emery, 2004). Similar complex societies are also found in dolphins (King & Janik, 2013), which are famous for their advanced cognitive abilities such as artificial ‘language’ comprehension and the ability of self-recognition (Marino, 2002). Highly developed cognitive capabilities are often linked to complex social systems, long life, and advanced communication skills (Marler, 1996; Pepperberg, 1999; Emery & Clayton, 2004; Dunbar & Shultz, 2007; Lefebvre & Sol, 2008), because species living in individualized social groups may require cognitive skills, solitary species do not need. Social animals have to maintain group cohesion; they must meet their own requirements but also coordinate their behaviour with the other members of their group depending on the group structure (Dunbar & Shultz, 2007). Since complex social skills can be a good predictor of cognitive complexity, we expect conures to perform well in string-pulling tests. In addition, foraging presents special challenges to conures. Their food sources are distributed non-uniformly in the environment and often spread out in discrete patches where fruits and seeds become ripe at different times (Freeland & Janzen, 1974). This time-varying food distribution forces the

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek S. Torres Ortiz et al. / Behaviour (2019) 5 parrots every day to decide for how long to forage in each patch and where to go next to forage efficiently (Walløe et al., 2015; Bradbury & Balsby, 2016). Furthermore, peach-fronted conures may feed on toxic unripe fruits and seeds like the closely related orange-fronted conures (Eupsittula canic- ularis). This is expected to be much more challenging than feeding on ripe non-toxic fruits and seeds (Bradbury & Balsby, 2016). It seems that there is always one bird in the flock who knows exactly when and where to go next. This ‘knowledgeable’ bird will climb to the top of the vegetation and give the “pre-flight” call, with which all flock will leave for the next food patch. To always have a bird in the flock with current knowledge of avail- able food sources may be one of the reasons for flock fusions. Consequently, there may be a close link between the fission-fusion behaviour, the complex communication system, and the complicated foraging habits of these parrots (Walløe et al., 2015; Bradbury & Balsby, 2016). This is another argument for the prediction that conures have better cognitive abilities and, therefore, will perform better in the string-pulling test than many other parrot species. To test this prediction, we studied the behaviour of peach-fronted conures in an assay of the six classical string-pulling tasks mentioned above to see if they show goal-directed behaviour, whether they rely on perceptual cues or trial-error learning to solve the tasks, and if they understand the concepts of physical continuity and connectedness. In addition, we performed a seemingly more difficult task that has tested in ravens but never in Psittaciformes: the pulley configuration. This configuration consisted of a string attached to the perch as in the usual tasks, but it was suspended upwards between the cage bars and over a second perch outside the cage such that the bird must pull the string down to move the reward up and within reach. Only ravens (Corvus corax) have been tested with this configuration (Heinrich & Bugnyar, 2005) and only experienced animals on the string-pulling task were able to retrieve the reward when presented with the pulley configuration. We predicted that peach-fronted conures could also solve this task after being exposed to all the classical previous string-pulling tests. So, the present study not only adds a new species with completely different foraging habits to the existing body of literature on string-pulling in birds, but also adds data on a variation of the string-pulling tasks that has never been previously tested with parrots.

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2. Materials and methods 2.1. Experimental animals We tested four peach-fronted conures (Eupsittula aurea), two males (M1 and M2) and two females (F1 and F2). The birds hatched in captivity in April 2014 and were brought to the laboratory six months later. During their time at the University of Southern Denmark (SDU), the parrots were raised in an aviary (for detailed information see housing conditions below) and were provided with branches and toys, but never exposed to toys with strings or just strings. Both males were from one clutch and the females were from another clutch. Data collection for the string-pulling experiments were conducted from November 2015 to March 2016 when the birds were between 18 and 23 months old. The parrots came from private breeders and were not accustomed to the presence of humans. They were also reluctant to approach and interact with every new object or stimulus presented to them. Such initial neophobic reac- tions are characteristic of most parrot species (Mettke-Hofmann et al., 2002). To avoid fear or neophobic behaviours affecting the results, an exhaustive training program was conducted during the eight months preceding the experiments. Using operant conditioning techniques (Hurley & Holmes, 1998), the training consisted of their habituation to human presence and of volun- tarily climbing into different cages. Additionally, on the last two days prior to conducting the experiments, each bird was habituated to strings in their home cages. A short (0.5 cm) string was attached around their perch, so they could explore and nibble it but there was no loose end for them to pull on in any way (see Figure 1a). No food was involved during the string habituation period. Such a habituation period is often used prior to testing neophobic animals (Heinrich & Bugnyar, 2005; Krasheninnikova et al., 2013). After this, we were able to manipulate the string setups while the experimental birds remained calm. 2.2. Housing conditions The study was conducted in a customised parrot room (5 × 5 × 3m)at the Department of Biology, SDU. This separately ventilated room was on a 12-h light-dark photoperiod and kept at a constant temperature of 27°C. The parrots were kept in same-sex sibling pairs in neighbouring home cages, each of which were 94 cm high, 82 cm wide and 54 cm long. After the experiment,

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Figure 1. Different arrangements of the strings in six of the seven tests. The strings with food reward at the end (open ellipses) were hanging by gravity, except for the slanted, crossed, and broken string conﬁgurations, where the strings were kept in position with very thin silk strands, almost ‘invisible’ to the human eye. The distances are not to scale but true distances are indicated. (a): a short (0.5 cm) string tied with a knot to the perch and used for string habituation prior to proper experiments. the parrots were transferred to a larger aviary (3 × 3 × 3 m). Here they were provided with a variety of toys, branches and perches and had constant visual and acoustic contact with one another. Toy ropes were very thick (2–4 cm in diameter) and it is therefore unlikely that the parrots would associate them with the thin strings in the string-pulling task. Thus, the experiments were performed with naïve birds, which could not have learned to solve the tasks prior to this study, and none of the subjects had ever been exposed to a string- pulling task before. The parrots were fed every day with a mixture of pellets, and water was provided ad libitum. On testing days, the birds were fed their regular number of pellets but we kept their favourite treat, the millet spray, as food rewards for the experimental testing. 2.3. Experimental setup The string-pulling experiments were performed in a separate empty cage of the same dimensions as their home cages but with only one central perch (Figure 2). The parrots were only provided with water to avoid distracting the bird from focussing on the task. To avoid observational learning from the

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Figure 2. Diagram showing the arrangement of the two webcams separated by 90°, facing the string arrangement on the perch and from the end of the test perch (not to scale), respectively. This example illustrates the multiple string geometry with food reward on string number two. other individuals, we had the experimental bird visually isolated from the others with removable polystyrene walls. The birds’ behaviour during experiments was recorded in real time with two webcams (Logitech Carl Zeiss Tessar HD 1080p) arranged orthogonally and connected to a laptop computer outside the parrot room. This was done to avoid the presence of an observer in the parrot room during the test trials, thus reducing the danger of bias in the bird’s responses due to intentional or unintentional cues given by the observer (‘the clever Hans effect’; see, e.g., Hediger, 1981). For each experimental string conﬁguration, we positioned the 2-mm diameter woollen strings centrally on the perch inside the cage where the experiments were conducted (Figures 1 and 2). Each string was 40 cm long (i.e., about double the body length of the birds), except for the ‘long string’ experiment, where the string length was 60 cm. To reduce time between trials when changing the position of the food reward (the bait), we attached a 2.5 cm snap hook to hold the food at the end of the strings. For the slanted,

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek S. Torres Ortiz et al. / Behaviour (2019) 9 crossed, and broken strings tasks, very thin silk threads were used to keep the strings in place against gravity (Figure 1). As previous studies had used such silk threads and did not detect any effects on the birds’ behaviour, we find them unlikely to confound the present results. 2.4. Testing procedure A trial started when the bird climbed down to the perch and appeared ready to solve the task. The trial starting time was later read from the video recordings. The trial was defined to have ended when the experimental bird either retrieved the food reward or when 10 min had elapsed. For the setup with a ‘pulley’ (see below) the time limit was set to 15 min as this task was deemed more difficult than the other ones. Due to the curiosity and exploratory behaviour of parrots (Demery et al., 2011), we decided to define the bird’s first choice for all tasks as the first string that it touched and subsequently pulled on. In cases where the bird only touched the string with its beak but did not pull it in, that string was not considered a choice. ‘Touched’ was defined as the action of the parrot’s beak touching the string but not moving it in any way. ‘Pulled on’ was defined as the action of the parrot’s beak holding the string and moving it such that the end of the string would come closer to the parrot. We did not use the forced-choice procedure in this experiment, so the subjects could still retrieve the reward when their initial choice was incorrect. A task was considered solved when the parrot was able to choose the correct string more often than predicted by chance. The experimental bird would enter the experimental cage prior to each trial. Between trials, we always held all strings together when we attached the new food reward to one of the strings and always released all strings simultaneously, after which the experimenter left the room. Meanwhile, the bird was allowed to watch due to the difficulty of moving birds back and forth between two cages. These procedures were followed to make sure that the experimental bird did not form a rule to always choose the string that had been rewarded in the previous trial or the one last touched by the experimenter during preparation for the next trial. The position of the food rewarded string (and its colour when different coloured strings were used) was randomized using the MatLab script ‘1 + floor(4 × rand(1,20))’ with the single extra rule: the food reward could not be on the same string for more than two trials in a row. Trials that did not live up to this extra rule were erased from the protocol.

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2.5. String-pulling tasks 2.5.1. Task 1: single string Only one trial of the single string task was conducted because all conures immediately succeeded (Figure 1). It had been deemed a necessary control in order to test the birds’ reaction to a single string, as well as their ability to pull up a baited reward. 2.5.2. Task 2: multiple strings Four strings of the same colour were used in the 20 trials. We considered it unnecessary to make the task easier by using different colours, since most of the previously tested parrot species understood this conﬁguration (Heinrich & Bugnyar, 2005; Werdenich & Huber, 2006; Schuck-Paim et al., 2008; Krasheninnikova et al., 2013; Jacobs & Osvath, 2015). The distance between the four strings was 7 cm (Figures 1 and 2). We decided to use four strings instead of two (as in previous studies) to get a clearer impression of the parrots’ understanding of the task. This meant that even if pulling the correct string was self-rewarding, the parrots needed to understand the string as a means to obtain the treat with a guessing probability of 0.25. The baited string position was randomized. 2.5.3. Task 3: slanted strings Two strings, coloured orange and blue, respectively, with the bait attached to one of them were both angled off to the right side by very thin silk threads. The food reward was located directly below the attachment of the empty string to the perch (Figure 1), such that the bird would need to understand that the string and not the vertical and closer position was the key to retrieve the bait. The strings had different colours to facilitate the task for the parrots (Krasheninnikova et al., 2013). With different colours, visually following a string would likely make the task easier and would not affect the task, since the purpose was to investigate if the parrots understood the connection between bait and string and the string as the means to retrieve the food reward. Both the colour and position were switched over the 20 trials following a Gellermann series (Gellermann, 1933), which is a pseudo-randomization of the stimulus presentation, to avoid a preference for colour or side. This meant that the food and the string colour were positioned such that neither the same string colour and/or position would repeatedly remain the correct choice, nor would there be an obvious stimulus pattern, such as a continuous alternation between the orange and blue strings being the correct choice (Gerard et al., 2014).

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2.5.4. Task 4: crossed strings To further establish if the birds’ choice of string was determined by the spatial or the functional relationship between string and food, we performed 20 trials using the crossed-strings configuration (Figure 1). Similar to Task 3, the bait was located directly below the attachment point of the unbaited string, but the visual continuity of the strings was more difficult to follow, since the strings were crossed. To ensure that the bird could follow the string from the perch to the bait, we again used strings of different colours: one blue and one orange. Again, both the colour and string position were switched following a Gellermann series (Gellermann, 1933) to avoid the birds basing their decision on either colour or string position. 2.5.5. Task 5: broken string For the broken string task, we tested if the experimental bird understood whether or not objects are physically connected. We made 20 trials with each bird. In these trials, the string colour was irrelevant, and therefore both strings were orange. Two rewards were present, one attached to one of the strings and another one suspended mid-air with thin silk threads. The distance between the end of the broken string and the food reward was 5 cm (see Figure 1). 2.5.6. Task 6: pulley In the pulley task, the conures had to pull the string downwards to move the food reward upwards and within reach for five trials of 15 min duration per trial. The string was attached to the perch as in the previous tasks but instead of hanging directly down by gravity, it was suspended upwards between the cage bars and over a second perch (Figure 3). Here we wanted to test the birds’ reaction to a stimulus configuration that was similar to, but different from, their previous experiences, and to examine their capacity to generalize information and transfer skills from the previous experiments. The behaviour sequence to solve this task was similar to solving tasks 1–5, so the performance was expected to be similar. 2.5.7. Task 7: long string A single 60 cm long baited string was hung from the perch. It was long enough that the birds could either retrieve the food reward from the perch by pulling the string up, as in Task 1, or by reaching for it when standing on the cage floor, since this species is believed to forage also on the ground (Sick

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Figure 3. Pulley conﬁguration: (A) Setup drawn to scale and (B) dimensions of the setup (not to scale).

& Barruel, 1984). To get an impression of their problem-solving flexibility and perseverance (defined as persistence in continually doing something de- spite difficulty or delay in achieving success), we tested if the parrots would change their behaviour to get the reward. When they faced this configuration, they had already pulled up a string 81 times. Therefore, this task was only repeated ten times.

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2.5.8. Task 8: multiple pulley Two strings of the same colour were positioned similarly to the pulley con- ﬁguration with one of the strings being baited (Figure 4a). The position was switched over the 20 trials following a Gellermann series to avoid a side preference. With this task, we wanted to test the birds’ performance when the multiple-choice task had a frontal view instead of a view from above as in task 2, multiple strings (Figure 1). We taught F1 and F2 to solve the pulley task by solving it in front of them and after that, we could test them with the multiple pulley (Task 8) and with the broken pulley (Task 9). 2.5.9. Task 9: broken pulley Two strings of the same colour were placed in a pulley arrangement. Both strings were baited, but only one of them was attached to the food (Fig- ure 4b). The goal of this test was to compare the results with the broken string task (Task 5) and see if the birds had a clearer understanding when the problem was presented in front of them rather than below. The position was switched over the 20 trials following a Gellermann series to avoid a side preference. 2.6. Video analysis Prior to data acquisition from the video recordings in Tasks 2–5, we made an ethogram of all types of behaviour observed during a selection of the trials (trial number 1, 2, 19, and 20). Partly in accordance with Werdenich & Huber (2006), all behaviours were sorted into three categories: “Efﬁcient”

Figure 4. Conﬁgurations for trials with two pulleys. (A) Photograph of the multiple pulleys during testing, and (B) photograph of the broken pulley during testing. Initially, the food rewards were at the same distance from the ﬂoor but pulling the chosen (and correct) string the parrot has moved it upwards in the photos.

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(those behaviours contributing to retrieval of the reward by bringing it closer to the bird), “Inefficient” (those delaying the retrieval of the reward by not moving it or moving it further away), and “Exploratory” (behaviours involv- ing approach to and observation of the strings but having no effect on the position of the reward relative to the bird; see Table A1 in the Appendix). Using the ethogram, the video recording for each trial, for each test, and for each bird was carefully analysed. The starting time of each trial was defined as the moment when the animal first sat on the perch, and the ending time was defined as the moment when the animal retrieved the food in its beak. Start and end time could be determined with a precision of ±1 s, which allowed calculation of trial duration with a precision of ±2 s. In addition, all behaviours performed during the trial were listed in order of occurrence. 2.7. Statistical analysis All statistical analyses were conducted using R (Version 0.99.491 — 2009– 2015; R Foundation Core Team, 2015). For the analysis of the single string test, the video of the first trial was analysed and all the behaviours were listed by order of occurrence. For Tasks 2–5, 8 and 9, we tested whether the choice of the parrots was different from random by fitting a General- ized Linear Mixed Model (GLMM) with Binomial error (see Table 1), with parrot identity as a random factor, with no fixed effect; in other words, this model shows if the intercept is significantly different from 0.5 or random distribution (i.e., a 50% chance of success and 50% chance of failure). For Tasks 2–5, a Generalized Linear Model (GLM) with gamma error structure was fitted to test for differences in duration among trials for each individual and task. The response variable was the time needed for solving the task (duration) and the explanatory variable was the trial number. For Tasks 2–5, the number of actions was analysed by comparing the first two trials with the last two trials out of 20 in order to see how the experimental bird’s behaviour changed throughout the session. This was tested by fitting a GLM with Poisson error structure to test the differences in the number of actions among trials for each individual and for each of the four tasks. The response variable was the number of actions and the explanatory variable was the trial number. For the analysis of the differences between the number of actions in each task, a GLMM with Poisson error structure was fitted with the parrot identity as a random effect. The response variable was the number of actions and the explanatory variable was the task. Tasks 6 and 7 were not analysed

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Table 1. Binomial probabilities from the GLMM model calculated to test if performance among trials for all individuals in each task was better than picking the string to pull by chance.

Task/Subject Success Success Probability Binomial Differences between ratios for ratios for of correct probability individuals the ﬁrst the second choice of random (individual probability ten trials ten trials choice of success)

Multiple strings M1 5/10 3/10 0.78 M2 9/10 4/10 0.77− ∗∗∗ 0.78 2.6 · 10 8 F1 3/10 7/10 (0.25) 0.78 F2 6/10 5/10 0.78 Slanted strings M1 6/10 8/10 0.76 M2 7/10 8/10 0.76− ∗∗∗ 0.76 9.0 · 10 6 F1 7/10 10/10 (0.50) 0.76 F2 7/10 8/10 0.76 Crossed strings M1 3/10 6/10 0.40 M2 3/10 5/10 0.40 0.40 0.076 F1 3/10 6/10 (0.50) 0.40 F2 3/10 3/10 0.40 Broken string M1 5/10 9/10 0.64 M2 6/10 4/10 0.64∗ 0.64 0.015 F1 5/10 9/10 (0.50) 0.64 F2 4/10 9/10 0.64 Multiple pulleys M1 9/10 9/10 0.83 M2 7/10 6/10 0.75∗∗ 0.69 0.0054 F1 8/10 9/10 (0.50) 0.80 F2 7/10 4/10 0.63 Broken pulley M1 7/10 3/10 0.52 M2 6/10 5/10 0.52 0.52 0.074 F1 6/10 6/10 (0.50) 0.52 F2 5/10 3/10 0.52

M = Male, F = Female. The number in parentheses besides the probability of correct ∗(∗∗) choice establishes the hypothesized probability of success. indicates (level of) signiﬁ- cance.

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek 16 Behaviour (2019) DOI:10.1163/1568539X-00003539 statistically since the result is solved/not solved and there are no choices. We tested the differences between tasks 2 and 6 (Multiple strings vs Multiple pulley) and tasks 5 and 7 (Broken string vs. Broken pulley) using a GLMM binomial model with ﬁxed effect for pattern and random effect for individual.

3. Results 3.1. Task 1: single string When a baited string was presented for the first time, all four birds immediately began to pull the string, showing that they have the physical capacity of string-pulling behaviour. Only one individual (F2) tried to reach the food by sitting on the side wall of the cage, but she returned to the perch after 45 s and eventually solved the task like the other birds. A detailed analysis of the behavioural action sequences of the experimental birds during their first attempt to solve this task is shown in Table A2 in the Appendix. Two individuals (M1 and F1) expressed only efficient actions, 13 and 20, respectively. The other male bird (M2) produced one inefficient action with 28 efficient actions before retrieving the food reward. The fourth bird (F2) showed exploratory and inefficient actions but these only represent 16% of her 51 behavioural actions until finally retrieving the food reward. The estimated binomial probabilities were always smaller than the actual outcome of all tests and for all birds, indicating that the birds were doing much better in these trials than just picking a string to pull by chance (see supplementary materials for details). 3.2. Task 2: multiple strings Two of the birds (M2 and F2) solved the multiple string task on their first trial and consistently solved the task during the remaining 19, with some mistakes in between. In contrast, the other two individuals (M1 and F1) failed their first attempt and the following ones. However, after five and eight trials for M1 and F1, respectively, almost all choices were correct. The duration for this task did not show any tendency towards decreasing or increasing for all 20 trials (GLM testing df = 79, z = 0.9, p<1; Figure 6). The combined results of all four parrots show that their readiness to pull the baited string was significantly greater than their choice of the empty ones (Figure 5; GLMM testing: df = 78, z = 5.6, p<0.0001; Table 1). Regarding duration, the mean time for solving this task for all individuals was 24.5 s

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Figure 5. Frequency of correct choices in four different tasks (multiple strings, slanted strings, crossed strings, and broken string conditions) reported as ratios. The ratio was calculated dividing the correct responses of each individual by the total number of trials. The horizontal lines at the value 0.25 for Multiple strings and value 0.5 for the remaining tests indicate where the data points were expected to be located if the parrots’ decisions were random.

(SE = 2.3 s). Differences in duration for the different individuals are not significant except for F2 that required more time to solve the task in later trials (M1: F = 3.8, df = 18, p<0.1, slope =−1.8; F1: F = 2.7, df = 18, p<1, slope =−1.0; M2: F = 0.4, df = 18, p<1, slope = 0.5; F2: F = 9.2, df = 18, p<0.01, slope = 1.0; Figure 6; see Table A3 in the Appendix). To understand how the birds’ behaviour developed throughout the ses- sions, the definitions in Table A1 were used to determine the efficiency of the birds’ actions by comparing their actions from the first two trials (1 and 2) with their actions from the last two trials (19 and 20; Figure 7). M1 and F1 significantly reduced both the total number of actions and the number of inefficient actions (Figure 7; GLMM testing for M1: df = 3, z = 6, p<0.0001; GLMM testing for F1: df = 3, z = 4.8, p<0.0001). For M2 there was a reduction in number of actions from the first trial to trial 19 followed by an increase in trial 20. Its number of inefficient actions decreased throughout the session (GLMM testing for M2: df = 3, z = 2.8, p<0.01). In contrast, F2 showed an increase both in the total number of actions and in the number of inefficient actions throughout the session (GLMM test df = 3, z = 13.4, p<0.001).

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Figure 6. Duration to complete each task for each individual as a function of trial number. The different lines indicate the time used by each animal to retrieve the food in each trial. Note that to accommodate all data points the ordinate of the crossed strings panel has a different scale than the other three.

3.3. Task 3: slanted strings

In the slanted strings task, three of the four birds solved the task on their first trial whereas the remaining individual (F1) solved the task on their second trial. All the parrots showed a high number of correct responses, and there was a significant difference between their disposition to choose the correct string over the incorrect one as their choices were highly non- random (Figure 5; GLMM test df = 78, z = 4.4, p<0.0001). There was not a significant change in duration to solve this task for all individuals (Figure 6;

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Figure 7. Bar diagram showing the number of efﬁcient, inefﬁcient, and exploratory actions for each animal in trials number 1, 2, 19 and 20 for the tasks multiple strings, slanted strings, crossed strings, and broken string.

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Table A3). The mean time to solve this task for all parrots was 19.2 s (SE = 1.6 s). All four birds performed a lower number of actions than in the multiple strings task (Figure 7; GLMM testing: df = 31, z =−2, p<0.05), most of which were efficient actions. M2 was the only individual showing a reduced number of actions throughout the session, but the reduction was not significant (GLMM testing: df = 19, z = 1.2, p>0.1). M1 and F1 remained relatively constant in their number of actions performed, whereas F2 was also close to constant, except for the last trial when there was a large increase in absolute number of actions, which included both exploratory and inefficient actions. 3.4. Task 4: crossed strings In the crossed strings task, all parrots failed on their first as well as the nine subsequent trials. After trial 10, the conures solved the task correctly by picking and pulling up the baited string. We found no significant differences in performance during the 20 trials (GLMM testing df = 78, z =−1.8, p<0.1). This indicates that the parrots’ decisions were random over the 20 trials. There was, however, a tendency to choose the non-baited string (see Figure 5). It appears from this analysis that M1, M2, and F1 showed a remarkable improvement in performance by reducing the duration of each trial (GLM testing for M1: df = 19, z = 2.8, p<0.05; GLM testing for M2: df = 19, z = 4.8, p<0.001; GLM testing for F1: df = 19, z = 3.3, p<0.01). In comparison, the remaining bird (F2) stayed almost constant (GLM testing for F2: df = 19, z = 0.003, p>0.1; Figure 5; Table A3). The average time to solve this task for all four parrots was 29.3 s (SE = 4.1). M1, M2, and F1 used a greater number of actions to solve the task during their first trial compared with the other tasks (Figure 7; GLMM testing df = 15, z = 16, p<0.0001). During the subsequent trials, all three birds notice- ably reduced both the total number of actions and the number of inefficient actions. 3.5. Task 5: broken string Three of the birds (M2, F1 and F2) failed the broken string task during their first trial. After two trials, however, three of the birds (M1, F1 and F2) solved the task and continued to solve it. The remaining individual (M2) performed the test correctly in half of the trials, showing no tendency of

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek S. Torres Ortiz et al. / Behaviour (2019) 21 improvement in the ability to choose the correct string. The combined results of all four parrots was non-random (GLMM testing, df = 78, z = 2.4, p< 0.05; Figure 4). The duration for solving this task was quite low from the first trial, with a mean time of 9.7 s (SE = 0.9) for all parrots, with only F2 showing a significant decrease in duration (Figure 6; Table A3). The number of actions was low in all trials for all four individuals and remained rather constant (Figure 7). 3.6. Task 6: pulley Males solved the task consistently for all five trials whereas the females gave up after the first unsuccessful trial and remained motionless until the 15 min had elapsed. On her first trial, F1 showed immediate interest in the pulley task for 37 s but then left the perch. After 180 s she tried again to solve it, again for 37 s, but then seemed not interested in the task anymore. Finally, 260 s later she tried to solve the task for 60 s. After that and during the next four trials, she did not try or even look at the setup until 15 min had elapsed. The second female (F2) only made two attempts: the first one for 160 s and after a break (lasting 120 s) she tried again for 25 s but failed and waited until time ran out; F2 did not show any interest during the next four trials. In contrast, both males kept on trying, until they got the reward (see Figure A1 in the Appendix). 3.7. Task 7: long string In all ten of the long string tasks, M1 and M2 did not change their pulling behaviour but immediately pulled up the string in the same way as in Task 1, to retrieve the food reward. In contrast, F1 changed its behaviour and took the reward from the string while standing on the floor in all trials, whereas F2 retrieved the reward from the floor on the first and ninth trial and pulled up the string in the same way as in Task 1 to obtain the reward during the remaining eight trials. 3.8. Task 8: multiple pulleys In the multiple pulleys task, M1 and F1 had a high number of correct responses, showing a clear understanding of the task (Figures 4a and 8). M2 succeeded in the task but not as consistently as M1 and F1. F2 performed the task correctly only for 50% of the trials, showing no preference for the

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Figure 8. Frequency of correct choices in the two pulley tasks (multiple pulleys and broken pulley conditions) reported as ratios. The ratio was calculated dividing the correct responses of each individual by the total number of trials. The horizontal line at the value 0.5 indicates where the data points were expected to be located if the parrots’ decisions were random. baited string. The GLMM test showed that the choice was non-random (df = 78, z = 2.8, p<0.01). The success rate was not significantly higher for the multiple pulleys than the multiple string task (GLMM testing df = 157, z =−0.6, p>0.1). 3.9. Task 9: (broken pulley) All four birds failed the broken pulley task (Figure 4b). It was not possible to detect a significant difference between correct and incorrect responses (Figure 8) and the choice by the parrots was random (GLMM testing, df = 78, z = 0.3, p>0.1). The parrots’ performance was not significantly different with the pulley configuration than in the traditional broken string task (GLMM testing df = 157, z =−1.5, p>0.1).

4. Discussion The aim of this study was to examine the cognitive skills and problem- solving behaviour of peach-fronted conures, as well as to investigate their behaviour in the pulley task, a string-pulling conﬁguration that has never previously been applied to parrots. The string-pulling test was used because

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek S. Torres Ortiz et al. / Behaviour (2019) 23 of its simplicity and because it has been widely used for testing many different animals. The results from the multiple strings task (Task 2) suggest that peach- fronted conures pulled the strings in a goal-directed manner, i.e., the subjects recognised the string as a means to obtain the reward. At the same time, it refutes the possibility that the pulling behaviour occurred because the action was rewarding in itself, which has been observed in other animal species (Schuck-Paim et al., 2008). To show goal-directed behaviour, the parrot needs to make its decision prior to acting and pick the right string on its first attempts without the possibility for trial and error learning. In our experiment, M2 and F2 solved the task on their first attempt and consistently during the first ten trials with few mistakes, suggesting that the task was not a real challenge for them. In contrast, M1 and F1 failed on their first trials but then suddenly started to perform correctly, indicating that these birds, had to gradually learn about the task through trial and error. F1 solved successfully seven out of ten trials in the second half while M1 did not perform above chance level, showing no understanding on the task. So, peach-fronted conures as a species have the capability to perform goal-directed behaviour but not all individuals followed this strategy to solve the task. Experimental animals may base their string-pulling decision on a proximity rule, by pulling the string attached closest to the bait. To investigate if peach-fronted conures understand the functionality of the strings’ configuration, we presented them with the slanted string condition (Task 3). Here the position of the bait was not closest to the correct string, to which it was actually attached; so, the parrot needed to visually follow the string from attachment to reward to pick the correct one. All birds had success rates significantly different from random for the slanted string task, indicating that they understood its functionality and that their performance was not based on a proximity rule, i.e., by always picking the string closest to the reward. While they could solve the other tasks, peach-fronted conures were unable to solve the crossed strings task (Task 4), even when differently coloured strings were implemented. Although this configuration is similar to the slanted strings task, the crossing of strings seemingly made the task too complicated, perhaps because the strings “converge their ways and are nonlinear” (Harlow & Settlage, 1934; Birch, 1945). Common ravens, hyacinth macaws, Lear’s macaws, and keas also had large difficulties in solving this task (Hein- rich, 1995; Werdenich & Huber, 2006; Schuck-Paim et al., 2008), whereas

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek 24 Behaviour (2019) DOI:10.1163/1568539X-00003539 spectacled parrotlets, galahs and cockatiels performed better than the peach- fronted conures in this task with differently coloured strings (Krashenin- nikova, 2013; Krasheninnikova et al., 2013). Several factors might affect performance in tasks such as crossed strings, one of them being age (Ja- cobs & Osvath, 2015). Older animals often perform better than young ones; most likely because of their larger experience in problem solving, their possible higher cognitive abilities, and the fact that they are less playful than younger animals (Mason & Harlow, 1961; Jacobs & Osvath, 2015). On the other hand, juveniles may sometimes be more successful in cognitive tasks because they can be more persistent (Vince, 1958). The young age (18–23 months) of the four peach-fronted conures tested here in the crossed strings task may explain their poor performance compared to, for instance, that of spectacled parrotlets where tested individuals were between one and eleven years old during testing. The broken string task (Task 5) was easily solved by the conures as shown by the short trial duration and their high percentage of correct responses right from the first trial. This suggests that these parrots understand the concept of connectedness between two objects (Piaget, 1954). This result is similar to the findings in a study on four other parrot species (Krasheninnikova et al., 2013; N = 3–10) but contrasts the results of a study on hooded crows (Corvus corone cornix; N = 10), which were unable to solve the broken string task (Bagotskaya et al., 2012). This result is rather surprising since corvids are otherwise characterized by extraordinary problem-solving abilities (Emery & Clayton, 2004). The pulley task (Task 6) was included because pulling a string downwards to move an object upwards is not as intuitively obvious as pulling a string upwards to move an object upwards. Still, the behavioural chain required to solve the task (grab string, pull, hold, and repeat) and the perceptual feedback of the food moving closer when touching the string is the same in the two situations. Previously, the pulley task has only been attempted with ravens (Heinrich & Bugnyar, 2005). In their study, only ravens experienced in other string-pulling tasks solved this task. Heinrich & Bugnyar (2005) suggested that the vertical string-pulling configurations were solved by means-end comprehension, because of the impossibility of naïve birds to solve the pulley configuration. Consequently, we assumed that after the 81 trials of pulling up the string, all our experimental and therefore experienced

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek S. Torres Ortiz et al. / Behaviour (2019) 25 birds would be able to solve this task easily and that it would not be possible to observe significant differences between individuals. However, only the two males spent sufficient time to solve the task, whereas the females only made brief unsuccessful attempts. The successful trials of the two males suggest that peach-fronted conures can generalize information from previous experiments and transfer skills to a novel situation but that not all individuals do it. Therefore, the mental abilities of the peach-fronted conures seem comparable to those of experienced ravens. Mammals are usually tested in a horizontal configuration with the strings in front of them, whereas birds are usually tested in a vertical configuration with the strings hanging below them. The latter configuration seems more challenging, since it probably requires better coordination and atten- tion than the former (Jacobs & Osvath, 2015). In addition to the classical string-pulling tests multiple strings (Task 2) and broken string (Task 5), we therefore designed two new string configurations, the multiple pulley and the broken pulley (Tasks 8 and 9). We hypothesized that the parrots’ performance would improve, since they now had a frontal view. Surprisingly, their performance was worse than before, maybe because they were unable to visually trace the paths of the strings due to the pulley configuration. The performance duration was not included in the analysis since at this point the parrots had been exposed to 86 string pulling attempts and any improvement in shortening the trial duration compared with tasks 2 and 5 could possibly be explained simply by an effect of task order. In any case, the vertical configuration was easier to solve for parrots, maybe because it is more ecologically relevant for them (Jacobs & Osvath, 2015). In the string-pulling test battery presented here, peach-fronted conures performed equally well than larger Neotropical parrots such as hyacinth macaws, and Lear’s macaws (Schuck-Paim et al., 2008). They were on par with ravens (Heinrich & Bugnyar, 2005; Werdenich & Huber, 2006) and with a ground-living parrot species, the kea (Werdenich & Huber, 2006) in these tests. Compared with rainbow lorikeets (Trichoglossus haemato- dus), green-winged macaws (Ara chloropterus), sulphur-crested cockatoos (Cacatua galerita; Krasheninnikova et al., 2013), and blue-fronted amazons (Amazona aestival; Schuck-Paim et al., 2008), conures performed better in the broken string test. Surprisingly, spectacled parrotlets but also galahs and cockatiels performed better than the peach-fronted conures in the crossed string condition

Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek 26 Behaviour (2019) DOI:10.1163/1568539X-00003539 with differently coloured strings (Krasheninnikova, 2013; Krasheninnikova et al., 2013). This result was not expected given similar foraging habits of the conures compared to those of the parrotlets, galahs, and cockatiels. Like them they spend much of their time foraging on the ground (Baker, 2003; Spoon et al., 2004; Krasheninnikova et al., 2013), thus the poorer performance of the conures in the crossed strings test is difficult to explain, as it is unlikely that the task requirements (i.e., visual-spatial abilities) favour the ecological niche of one species more than that of the other. To gain more insight into how the string-pulling tasks test for parameters such as fine motor skills and visual-spatial abilities (Magat & Brown, 2009; Krasheninnikova, 2013), it would be relevant to test spectacled parrotlets, galahs, and cockatiels with the pulley task and compare their performance with that of the peach-fronted conures. We predicted that peach-fronted conures would perform better in string- pulling tasks than many other parrots, since their complex social system with advanced communication to forage efficiently in time-varying food patches seems to require high cognitive abilities (Kamil & Roitblat, 1985). Our results, however, are mixed since these parrots performed better than some species but worse than others in the string-pulling tests. To elucidate how complex social systems and complex foraging ecology act as drivers of cognitive skills in parrots, we need to systematically test many more parrot species with a battery of well-defined cognitive tasks.

Acknowledgements All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. We are grateful to Thorsten Balsby and two anonymous reviewers whose comments improved the manuscript signiﬁcantly, and to Iain Stott, Josephine Goldstein, Owen Jones and Iris Adam for help with statistics. This project was funded by the Danish Council for Independent Research | Natural Sciences through grants to Ole Næsbye Larsen (DFF — 1323-00105) and Magnus Wahlberg (DFF — 4002-00536). The authors have no conﬂict of interest.

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Appendix

Figure A1. The duration to solve the pulley task as a function of the trial number for the two male parrots. The regression lines are derived from the GLM (df = 6, z = 16, p<0.0001). Both females failed to solve the task.

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Table A1. Action list and action sequences in the attempt to retrieve the bait.

Action number Action

Efﬁcient actions 1 Lands on the perch 2 Grasps the string with the beak 3 Lift up the string with the beak 4 Uses one foot to hold the string on the perch 5 Stretches up the body to gain more string 6 Grabs the string with the foot 7 Takes one or more steps sideways on perch holding the string with the beak 8 Pulls up the string with one foot while sliding it in the beak 9 Release the string from the beak to reach down again 10 Gains reward after having pulled up string Inefﬁcient actions 11 Drops the entire string after having pulled it up 12 Drops the string partially after having pulled it up 13 Flies off the perch Exploratory actions 14 Nibbles the string 15 Nibbles the perch

This is an extended and revised list of the original definitions made by Werdenich & Huber (2006). Definitions of Efficient, Inefficient and Exploratory actions are given in the main section of the paper.

Table A2. Action sequences of individual peach-fronted conures in their ﬁrst attempt to secure the food reward in the single string task.

Subject Action sequence

M1 1-2-6-9-2-6-9-2-6-9-2-6-10 M2 1-2-3-7-11-2-3-4-9-2-3-4-2-3-6-9-2-3-6-9-2-3-6-9-2-3-6-10 F1 1-2-3-4-2-3-6-9-2-3-6-9-2-3-6-9-2-3-6-10 F2 1-2-3-6-11-2-3-6-9-2-3-6-9-2-14-3-11-13-1-2-3-6-9-2-3-6-9-2-3-6-11-14-13-1-2- 3-7-6-9-2-3-7-6-9-2-3-12-2-3-6-10

See Table A1 for action types. Exploratory and inefﬁcient actions are given in bold. M = Male, F = Female.

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Table A3. Results from the General Linear Model used to test for differences in duration among trials for each individual and task.

Task Subject Result

Multiple strings M1 Mean = 27.6, SE = 5.8, F = 3.8, df = 18, p = 0.07, (20 trials per slope =−1.8 individual) M2 Mean = 31.8, SE = 4.6, F = 0.4, df = 18, p = 0.5, slope = 0.5 F1 Mean = 21.5, SE = 4.2, F = 2.7, df = 18, p = 0.7, slope =−1.0 ∗ F2 Mean = 17, SE = 2.3, F = 9.2, df = 18, p = 0.007 , slope = 1.0 Slanted strings M1 Mean = 20.7, SE = 3.4, F = 3.1, df = 17, p = 0.1, (20 trials per slope =−1.0 individual) M2 Mean = 20, SE = 4.4, F = 1.3, df = 18, p = 0.3, slope = −0.8 F1 Mean = 19.1, SE = 3, F = 0.1, df = 17, p = 0.7, slope = 0.2 F2 Mean = 16.8, SE = 1.6, F = 1.1, df = 17, p = 0.3, slope =−0.3 ∗ Crossed strings M1 Mean = 48.7, SE = 13.1, F = 6.7, df = 18, p = 0.02 , (20 trials per slope =−5.2 ∗ individual) M2 Mean = 24.7, SE = 6, F = 8.3, df = 18, p = 0.01 , slope =−2.5 F1 Mean = 22,9, SE = 6.5, F = 4.3, df = 18, p = 0.05, slope =−2.2 F2 Mean = 20.8, SE = 3, F = 1e−5, df = 18, p = 1, slope =−0.002 Broken string M1 Mean = 7.2, SE = 0.5, F = 2.5, df = 18, p = 0.1, (20 trials per slope =−0.1 individual) M2 Mean = 13, SE = 3.5, F = 0.7, df = 17, p = 0.4, slope = 0.5 F1 Mean = 7.5, SE = 0.5, F = 0.07, df = 16, p = 0.8, slope =−0.03 ∗ F2 Mean = 11.1, SE = 1.2, F = 4.7, df = 18, p = 0.04 , slope =−0.4 ∗ All tasks M1 Mean = 26, SE = 4, F = 9.5, df = 77, p = 0.003 , (80 trials per slope =−2. individual) M2 Mean = 22.4, SE = 2.4, F = 2.2, df = 77, p = 0.1, slope =−0.6

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Table A3. (Continued.)

Task Subject Result ∗ F1 Mean = 17.7, SE = 2.2, F = 5.4, df = 75, p = 0.02 , slope =−0.9 F2 Mean = 16.4, SE = 1.1, F = 0.2, df = 77, p = 0.7, slope = 0.08

Mean and standard error units expressed in seconds. M = Male, F = Female. ∗ Signiﬁcant result.

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