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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 Go to publication entry in University of Southern Denmark's Research Portal Terms of use This work is brought to you by the University of Southern Denmark. Unless otherwise specified it has been shared according to the terms for self-archiving. If no other license is stated, these terms apply: • You may download this work for personal use only. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying this open access version If you believe that this document breaches copyright please contact us providing details and we will investigate your claim. Please direct all enquiries to [email protected] 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 be- cause of its easy application and its potential to be applied to different taxa. © Koninklijke Brill NV, Leiden, 2019 DOI 10.1163/1568539X-00003539 Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek 2 Behaviour (2019) DOI:10.1163/1568539X-00003539 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 coordi- nation 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 connected- ness. 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 ani- mal 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 under- stand the concept of connectedness to solve this configuration. Animals with means-end understanding do not necessarily understand the concept of con- nection. 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 mul- tiple 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, bro- ken 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; Downloaded from Brill.com03/11/2019 07:10:33AM via Syddansk Universitetsbibliothek 4 Behaviour (2019) DOI:10.1163/1568539X-00003539 N = 8) passed all the string-pulling tests: multiple strings, slanted strings, crossed strings, and
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