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Psittacine cognition: Individual differences and sources of variation
Accepted Manuscript Title: Psittacine Cognition: Individual Differences and Sources of Variation Author: Victoria A. Cussen PII: DOI: Reference:
S0376-6357(16)30358-8 http://dx.doi.org/doi:10.1016/j.beproc.2016.11.008 BEPROC 3332
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Behavioural Processes
Received date: Revised date: Accepted date:
21-6-2016 13-11-2016 17-11-2016
Please cite this article as: Cussen, Victoria A., Psittacine Cognition: Individual Differences and Sources of Variation.Behavioural Processes http://dx.doi.org/10.1016/j.beproc.2016.11.008 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Psittacine Cognition: Individual Differences and Sources of Variation.
VICTORIA A. CUSSEN Department of Neurobiology, Physiology & Behavior, University of California, Davis
Correspondence: V.A. Cussen, Department of Neurobiology, Physiology & Behavior, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA (email: [email protected]; tel +1 (530) 752-0203; fax +1 (530) 752-5582.
Highlights
Psittacine cognition research originally focused on ‘proof of capacity’
Three species account for approximately half of all parrot cognition research
The number of psittacine species and individuals tested is expanding
Intraspecific variation is common in psittacine cognition research
Non cognitive factors such as personality may play a role in variation and should be controlled for in study design
Cognitive normal ranges need to be established for each species and assay
Abstract Both the number and breadth of avian cognition studies have expanded in the past three decades. Parrots have a long history as subjects in avian cognition research. This paper summarizes results from a number of parrot species tested on basic learning, and physical & social cognitive processes, with an emphasis on individual differences. Early psittacine studies were aimed at demonstrating a particular cognitive ability existed in a given species. Because of this proof of capacity focus, early studies typically included only a single individual or a dyad of parrots. Existing reviews of parrot cognition tend to focus on a particular cognitive component in a single species, or even a single individual. Despite the narrow focus, results from increasing sample sizes show intraspecific variation across a variety of cognitive assessments and parrot species. Intraspecific variability in performance on cognitive tasks highlights the need for establishing a cognitive normal range for a given species and process. To accomplish this, large numbers of individuals need to be tested and non-cognitive sources of variability need to be controlled. Once species typical cognitive normal ranges are established, cognitive comparisons can be made between parrot species and between parrots and other taxa.
Keywords: parrot; avian cognition; personality; individual differences; cognitive normal range
Introduction Birds have long been a staple of cognition research (e.g. Gossette et al. 1966), with the past three decades seeing an expansion in both the number and breadth of avian cognition studies (Willemet 2013). Fields of inquiry such as cognitive ecology are posing new questions about the adaptive function (Dukas 2004, Lefebvre et al. 2004, Morand-Ferron et al. 2015), fitness benefits (Boogert et al. 2011, Morand-Ferron et al. 2015, Sol et al. 2007) and possible trade offs (Healy 2012) of cognitive abilities. Research emphasis has shifted from generalized learning principles in pigeons to a broad range of cognitive processes across species (see reviews of episodic-like memory: Salwiczek, Wanatabe, and Clayton, 2010; navigation: McMillan et al. 2015; scatterhoarding: Pravosudov and Roth 2013; foraging: Healy and Hurly 2013; innovation: Griffin and Guez 2014).
Still, particular taxa remain more heavily represented in the literature than others. The Corviade family is an example. Since the string pull test pioneered by Bernd Heinrich (1995), corvids have been tested on a variety of social, physical, and general cognitive processes. Episodic-like memory (scrub jays, Clayton and Dickinson 1998), insightful tool use (New Celedonian crows, Taylor et al. 2011, but see Seed and Boogert 2012), and social cognition (ravens, Bugnyar 2011; 2013) are well documented (for reviews see Emery and Clayton 2004, Taylor 2014). The brains of some corvid species have enlargements in areas involved in higher order cognitive processes (relative to overall brain size, referred to as ‘relative brain size’, Iwaniuk et al. 2005). These brain areas are though to function in a similar way to the primate neocortex, providing the neural
substrate for advanced cognitive abilities (Reiner 2005, Jarvis et al. 2005, Güntürkün 2012). Parrots, like corvids, possess a large relative brain size that is equivalent to that of some primate species (Iwaniuk and Hurd 2005) and parrots are similarly regarded as cognitively sophisticated (Emery 2006). The parallel interest in corvid and psittacine physical cognition recently led to a direct comparison between those taxa (Auersperg et al. 2011).
Parrots have a long history as subjects in avian cognition research, at least partly due to Irene Pepperberg’s pioneering work with Alex the African grey parrot (see below). Early psittacine cognition research was characterized by ‘power studies,’ aimed at demonstrating a particular ability existed in a given species (Pepperberg and Funk 1990). In other words, a single individual exhibiting a given cognitive ability provided evidence that the capacity existed within that species - regardless of whether or not it was widespread. Because of this proof of capacity focus, early studies typically included only a single individual or a dyad of parrots. Unlike corvids, where reviews exist that span cognitive processes and/or species, reviews of parrot cognition tend to focus on a particular cognitive component in a single species, or even a single individual.
Finally, across taxa authors are beginning to explicitly examine individual variation and report the magnitude of that variation on experimental tasks (e.g. Guillette et al. 2011, 2015, Croston et al. 2016). Characterizing the cognitive abilities of a species requires developing a cognitive normal range. In much the same way that there are normal ranges for phenotypic parameters such as height, longevity, or heart rate in a species, the
cognitive normal range is the species-typical magnitude of between-subjects variation on a given cognitive process. Sample sizes in psittacine cognition studies have increased across time, providing descriptive information on intraspecific variation in task performance. However, individual differences have yet to be systematically investigated in parrot species.
This paper considers three decades of psittacine cognition research and summarizes the distribution of parrot species and individuals investigated, intraspecific differences reported, and possible causes of variation in test performance.
Psittacine Cognition Research Perhaps no individual bird is as emblematic of avian cognition research as Alex the African grey (Psittacus erithracus) parrot. Alex’s career as Irene Pepperberg’s test subject spanned three decades; their partnership is chronicled in the popular press book, The Alex Studies (Pepperberg 1999). Pepperberg’s work with Alex is summarized in multiple review articles: studies covered the development of basic cognitive processes using Piagetian stages (reviewed in Pepperberg 2002), referential learning and abstract category formation (reviewed in Pepperberg 2013), and numerical competence (reviewed in Pepperberg 2006a). Those early studies helped to catalyze interest in and expand understanding of psittacine cognition.
Subsequent research efforts have expanded the types of cognitive processes examined (e.g. Pepperberg 2004), the number of individual subjects included (e.g. Giret et al.
2010), and the parrot species studied (e.g. Brown and Magat 2011a). Table 1 lists 71 psittacine cognition studies, including species, sample size, cognitive process investigated. The studies listed cover 29 species of parrots. African grey parrots dominated early papers: 12 of 20 papers published prior to 2005 used African greys as their subjects, compared to a quarter of the 51 studies published after 2005. Both kea (Nestor notabilis) and orange-winged Amazon parrots (Amazona amazonica) have surpassed African greys as the most common study species. Psittacine cognition research programs now exist in Australia, Europe, South America, and the United States. Work done with wild and captive keas at the Konrad Lorenz Institute is an example of research assessing cognitive processes in a novel study species. The group has investigated innovation, social learning, tool use, and causal reasoning on a variety of tasks (for a review of research on ‘technical intelligence’ in keas, see Huber and Gajdon 2006).
Variation in Psittacine Cognition Since the late 1990s parrot cognition study sample sizes have generally increased, although the number of subjects remains highly variable across studies (see sample sizes in Table 1). Results from studies with larger sample sizes indicate that while a particular cognitive capacity may exist somewhere within a parrot species, it is not necessarily widespread (Schuck-Paim et al. 2009). For example, a study of innovation in wild kea found only 5 of 36 individuals successfully foraged from closed garbage cans (an assessment of physical cognition), and even these lid-opening individuals failed to open the lids on approximately 90% of their attempts (Gajdon et al. 2006). Krasheninnikova (2013) found the number of string pull tasks on which individual Galah cockatoos
(Eolophus roseicapilla) met criteria ranged from 2 to 5 tasks across subjects. Further, individuals that did complete the task significantly differed in the technique they used (Krasheninnikova 2013). African greys parrots’ performance on inference by exclusion tasks also ranged widely between individuals, by over 30% in some task conditions (Mikolasch et al. 2011). Even captive-bred siblings,vary in their performance on cognition tests (Piagetian development tasks, yellow crowned parakeets [Cyanoramphus auriceps] see Funk and Matteson 2004).
Despite growing evidence of variation in cognitive abilities (Thornton and Lukas 2012) the mechanisms mediating avian intraspecific variation are currently unknown (Griffin and Guez 2014). One possible mechanism is related to how information processing. In mammals, information can be preferentially processed in one of the two cerebral hemispheres and the strength of the hemispheric dominance (‘cerebral lateralization’), is linked to cognitive function and behavioral performance (Rogers 1996). Similar processing asymmetries occur in avian brains, which lack hemispheres (Brown and Magat 2011b, Rogers 2009). Cerebral lateralization can be indirectly measured by motor lateralization, or limb preference. The strength of limb preference in parrots appears to be correlated with cognition. For example, more strongly lateralized birds performed better on both means end discrimination (Magat and Brown 2009) and spatial memory (Cussen and Mench 2014a) tasks. Those studies report both species differences and intraspecific variation in the strength of motor lateralization and cognitive performance. An important first step in understanding mechanisms of cognitive variability is to characterize the
species-typical cognitive normal range for a given task (e.g. Cole et al. 2012), and to determine how much of the variability is related to non-cognitive factors.
Non-Cognitive Contributors to Variability In addition to differences in cognitive ability, variation in results can be caused by noncognitive factors that influence individual task performance. Morrand-Ferron and colleagues (2015) identified the following four non-cognitive factors that could contribute to variability in cognition studies: perceptual and motor biases, motivation, personality, and environmental factors. For example, both keas (Miyata et al 2011) and orange-winged Amazons (Cussen and Mench 2014a) showed side biases when interacting with the test apparatus. Keas are neophilic and readily interact with novel objects (Huber and Gajdon 2006), but many other parrots species tend towards neophobia (e.g. African greys, Péron et al. 2011). The correlation between neophobia (a personality trait) and problem solving ability conflicts across studies (see review in Griffin and Guez, 2014). But individual differences in personality can influence cognition (e.g. susceptibility to attention biases, Cussen and Mench 2014b) and learning strategies (Mathieu et al. 2012), although much remains to be clarified about this relationship (Griffin et al. 2015). These and the other non-cognitive factors discussed below are important variables to quantify and/or control when designing or interpreting psittacine cognition research. Otherwise, incorrect inferences can be drawn about a species cognitive normal range or about interspecific comparative cognition.
Testing Environment: Krasheninnikova and Schneider (2014) tested orange-winged Amazons on a series of seven string pull tasks. Some parrots were tested individually and others were allowed to interact with the task in a social condition. Parrots in the social condition had a higher participation rate and the majority of subjects completed all string pull tasks. Only half of the individually tested parrots completed all tasks. It is possible that testing parrots in social settings reduces neophobia when interacting with a novel task and contributes to success (though stimulus enhancement may play a role, e.g. Mikolasch et al 2012). Either way, the social environment during cognitive tests can influence parrots’ success.
Conspecific influence can also depend on the identity of the social group members. African grey parrots chose to interact with a cooperative string pull apparatus preferentially depending on the identity of the available partner (Péron et al. 2011) and reciprocity was influenced by dominance rank of the individual being tested (Péron et al. 2013). Dominance rank also played an important role in a cooperation task given to keas, with dominant individuals able to monopolize the reward and coerce subordinates to assist with the task (Tebbich et al 1996).
Sex Differences: Sex can contribute to variability in test results (Healy et al. 2009) but sex differences remain largely unexplored in parrots, likely because of small sample sizes. While no female keas were successful in opening garbage lids (Gajdon et al. 2006), only of a minority of males were successful and the overall low success rate makes sex comparisons difficult. Krasheninnikova and Wanker (2010) directly tested for sex effects
and found no difference on a string pull task in spectacled parrotlets (Forpus conspicillatus). Many studies had too few subjects, or subjects of unspecified sex, to test for sex effects directly (see sex ratio in Table 1).
Subject History: Unlike work in other taxa (e.g. Pravosudov and Roth 2013), psittacine cognition research is dominated by comparative cognition approaches in captive settings. This may reflect the complex testing paradigms, which can require extensive training and lend themselves well to laboratory studies (Giret et al. 2010), or may result from the general difficulty of assaying cognition in the field (Morand-Ferron et al. 2015). Wild, free-living parrots were subjects in 7 of the 71 studies indexed in Table 1, with one other study using wild caught, captive subjects. A further 15 of the 71 studies included subjects with a mixture of backgrounds (wild caught and captive bred), and several more included captive bred parrots that were either parent- or hand- reared (4 and 18 studies of 71, respectively). The majority of studies (n=26) used captive subjects whose backgrounds were either unknown or unreported (see Status in Table 1). Early life experience is known to have significant effects on parrot development (Fox and Millam, 2004), making subject background an important variable to report and to consider in analyses.
The effect of subject history is evident in differential performance between laboratoryreared and wild conspecifics, a phenomenon that is documented in several species (Huber and Gajdon 2006) from cognitive tasks to physiological parameters (e.g. Calisi and Bentley 2009). For example, captive kea tested on a physical cognition assay readily learned the required task; the majority of the kea solved it spontaneously and the
remaining birds learned the solution after it was demonstrated to them. However, only 3 of 21 color banded wild keas learned how to solve the same task, and then only after the experimenters trained a demonstrator bird (Gajdon et al. 2004). Variability in backgrounds is sometimes unavoidable, such as in zoo studies, but it is an important variable to consider when interpreting results, as life experience may confound the results of between species or subjects comparisons.
Inhibition of Response: Finally, several authors have raised the issue of impulsivity in parrots (e.g. de Mendonça-Furtado and Ottoni 2008, but see Koepke et al. 2015). The apparent inability to inhibit motor control was thought to impair performance on cognitive tests in several studies (Cussen and Mench 2014a, Péron et al 2011, Mikolasch et al. 2012). Explicitly testing inhibitory control across parrot species could aid in interpretation of results in the future (Liedtke et al. 2011).
Conclusion The large Psittacidae family (over 400 species, Joseph et al. 2004) is well suited to phylogenetic studies of cognitive abilities (Mettke-Hoffman et al. 2002) and mechanisms underpinning cognitive variability (Mettke-Hoffman 2014) . Still, the vast majority of studies, with a few notable exceptions (e.g. Auersperg et al. 2014, Brown and Magat 2011a, Magat and Brown 2009), involve a single parrot species. Psittacine cognition research generally is limited to African grey parrots, kea, and orange-winged Amazon parrots. Those three species account for almost half of the parrot subjects listed in Table 1. In addition to increasing the number of species investigated, testing should be carried
out in both the wild, where normal ecological and developmental conditions occur, and in the laboratory, where non-cognitive factors can be better controlled (Rowe and Healy 2014, Sulikowski and Burke 2015, Brown & Magat 2011a) Newly available automated operant devices can be used to test cognitive processes in free-living individuals (e.g. Morand Ferrond et al. 2013). Identifying and controlling non-cognitive factors such as rearing history, sex, age, previous testing experience, etc. (for an example, see Auersperg et al. 2015) will allow for partitioning of variance that does not reflect variation in cognitive ability.
In 30 years of research effort, 462 unique individual parrots (28 African greys, 55 orangewinged Amazons, and 128 keas) were used as subjects in cognition research.. Birds of a given species vary in ways that have important consequences for their behavior and overall fitness (Dingemanse and Wolf 2010, Smith and Blumstein 2008) from physiological differences (Koolhaas et al. 2010) to differences in behavior (van Oers et al. 2005) and decision-making (Morgan et al. 2014). The shallow subject pool hampers understanding of the distribution and adaptive value of cognitive processes within parrot species. Determining a cognitive normal range, or the intraspecific variability on a particular cognitive task, requires testing large numbers of individuals (e.g. Cole et al., 2011). Focusing research effort on the three commonly-studied parrot species (African grey, kea and orange-winged Amazons) and selecting cognitive tasks that have existing data from the largest number of unique individuals would be a good starting point for expanding the number of subjects tested in support of developing cognitive normal
ranges for those tasks. Then these ranges can be used to make meaningful comparisons between parrot species, and between psittacines and other avian taxa. Acknowledgments I am grateful to Professor Thomas Coombs-Hahn for providing support while writing this manuscript. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Table Table 1: Psittacine cognition articles. A variety of cognitive processes have been studies, mainly in African grey, Kea, and orange-winged Amazon parrots. Sample sizes have generally increased over the years, but remain highly variable and often small. BASIC PROCESSES: Status* Sex Sample Assessment Author Species M:F** (n) Giret et al. African grey (Psittacus 4 1:1 2 Categorization (2009a) erithacus) Referential label Giret et al. 6 NR 10 learning (2010) African grey Inference by Mikolasch et al. 5 4:3 7 exclusion (2011) African grey Local Mikolasch et al. 5 4:3 7 enhancement (2012) African grey Delay of 4 2:1 3 gratification Vick (2010) African grey Category Pepperberg 5 1:0 1 comprehension (1990) African grey Conjunctive label Pepperberg 5 1:0 1 comprehension (1992) African grey Category Pepperberg 5 1:0 1 comprehension (2013) African grey Delay of Koepke et al. 4 1:0 1 gratification (2015) African grey Piagetian Pepperberg et 4 1:0 1 development al. (1997) African grey African grey, Illiger macaw (Ara maracana), Cockatiel (Nymphicus hollandicus), Parakeet (Melopsittacus undulates)
Blue fronted Amazon
N/A Orange-winged Amazon (Amazona amazonica)
5
5
N/A 3
N/A
4
Object permanence
N/A
Learning set generalization Piagetian Framework Review
5:8
Cognitive bias (attention bias)
1:0
1
12
Pepperberg and Funk (1990) de MendonçaFurtado and Ottoni (2008) Pepperberg (2002) Cussen and Mench (2014b)
Orange-winged Amazon Orange-winged Amazon Rainbow lorikeet (Trichoglossus moluccanus) Yellow-crowned parakeet (Cyanoramphus auriceps) Yellow-crowned parakeet Yellow-headed Amazon (Amazona oratrix)
3
5:8
12
5
1:1
2
Learning set acquisition & breaking, long term memory Analogical reasoning
12
Win-shift/winstay strategy
5
NR
6
7:4
11
6
NR
11
Piagetian development Piagetian development Discrimination & reversal learning Foot preference & lexicon size Laterality of foot use Knowledge transfer Means-end comprehension Discrimination discrete & continuous amounts Inferential reasoning
2
NR
2
African Grey
5
NR
524
23 Australian species
6
NR
1
Kea (Nestor notabilis)
5
5:1
6
8 Australian Species
5
NR
40
African Grey
4
2:1
3
African Grey
6
3:1
4
Status
Sex M:F
African Grey
4
2:0
2
African Grey
5
3:3
6
African Grey
5
1:0
1
Mirror tasks Inferential reasoning Numerical competence
African Grey
5
1:0
1
Zero-like concept
Cussen and Mench (2014a) Obozova et al. (2015) Sulikowski and Burke (2011) Funk and Matteson (2004) Funk (1996) Gossette et al. (1966) Synder and Harris (1997) Brown & Magat (2011a) Gajdon et al. (2013) Magat and Brown (2009)
Aïn et al. (2009) Pepperberg et al. (2013)
PHYSICAL COGNITION: Species
Sample Assessment (n)
Author Pepperberg et al. (1995) Schloegl et al. (2012) Pepperberg (2006) Pepperberg (2006)
Labels Means-end comprehension
Pepperberg (2006) Pepperberg (2012) Pepperberg (1994) Pepperberg and Brezinsky (1991) Pepperberg and Gordon (2005) Pepperberg and Shive (2001) Pepperberg (2004)
61
Play
Auersperg et al. (2014)
16
Means-end comprehension
Krasheninnikova (2013)
Auersperg et al. (2015)
African grey
5
1:0
1
African Grey -
5
1:0
1
African Grey
5
1:0
1
African Grey
5
1:0
1
African Grey
5
1:0
1
African Grey
4
1:0
1
African Grey Black palm cockatoo (Probosciger aterrimus), Kea; African grey, Black billed Amazon (Amazona agilis), Yellow billed Amazon (Amazona collaria), Goffin cockatoo (Cacatua goffiniana) Galah cockatoo (Eolophus roseicapilla), Cockateil Goffin cockatoo, Red shouldered macaw (Diopsittaca nobilis), Black headed caique (Pionites melanocephalus) Hyacinth (Anodorhynchus hyacinthinus) and Lear's macaw (Anodorhynchus leari), Blue-fronted Amazon (Amazona aestiva)
6
4:0
4
6 3
NR NR
Numerical competence Numerical competence Quantity discrimination Class concept Numerical competence
4
NR
22
Play
6
8:10
10
Means-end comprehension
Hyacinth Macaws
6
2:4
6
Tool use
Kea
6
6:0
6
Kea
N/A
N/A
12
Tool use Technical intelligence
Schuck-Paim et al. (2009) Borsari and Ottoni (2005) Auersperg et al. (2011) Huber and Gajdon (2006)
Review Kea
6
7:0
10
Kea
6
1:0
10
Kea
4
5:2
7
Artificial fruit Inference by exclusion Means-end comprehension
Kea, Macaw, Cockatoo
5
NR
10
Trap tube
58
Means-end comprehension
Orange-winged Amazon
PHYSICAL COGNITION: Species (cont’d) Spectacled parrotlet, Rainbow lorikeet, Green-winged macaw (Ara chloroptera), Sulphur crested cockatoo (Cacatua galerita) Yellow-crowned Parakeet
5
NR
Status
Sex M:F
5
NR
39
6
NR
11
Status
Sex M:F
Sample Assessment (n)
Means-end comprehension Means-end comprehension
Miyata et al. (2011) Schloegl et al. (2009) Werdenich and Huber (2006) Liedtke et al. (2011) Krasheninnikova and Schneider (2014) Author
Krasheninnikova et al. (2013) Funk (2002)
SOCIAL COGNITION: Species African Grey
5
0:1
African Grey
4
2:1
African Grey
4
2:1
African Grey
4
2:0
African Grey
4
2:0
African Grey
4
2:0
Sample Cognitive (n) Process Social context & vocalizations Discrimination of 3 vocalizations Use of experimenter 3 given cues Vocal learning – 2 social impact Reciprocity & 2 sharing Acquisition of human language 2 labels
Author Colbert-White et al. (2011) Giret et al. (2009b) Giret et al. (2009c) Pepperberg et al. (1999) Péron et al. (2013) Pepperberg and McLaughlin (1996)
African Grey
4
2:1
3
African Grey
4
1:0
1
African Grey
4
1:0
1
African Grey Crimson rosella (Platycercus elegans)
6
3:0
3
1
NR
182
Cooperation Vocal learning – social impact Reciprocity & sharing Acquisition of human language labels
Green-rumped parrotlet (Forpus passerinus)
1
NR
34
N/A Social transmission tool manufacture Social transmission unique calls
Kea
5
5:7
1
Social learning
Kea
1
23:12
36
Social learning
Kea
6
5:2
7
Cooperation
Goffin cockatoo
4
6:6
12
Péron et al. (2011) Pepperberg et al. (2000) Péron et al. (2014) Pepperberg and Wilcox (2000) Ribot et al. (2012) Auersperg et al. (2014b) Berg et al. (2011) Huber et al. (2001) Gajdon et al. (2006) Tebbich et al. (1996) Gajdon et al. (2004) Moura et al. (2014)
1 NR 21 Social learning Kea Gestural Orange-winged 1 8:8 32 communication Amazon Yellow-naped Parrot Dahlin and (Amazona 1 1:1 38 Syntax in duets Wright (2012) auropalliata) *Status: 1=Free-living, 2=Captive: Wild caught, 3=Captive Bred: Parent reared, 4=Captive Bred: Hand reared, 5=Captive: Breading & rearing unknown/unspecified, 6=Captive: Mixed backgrounds **Sex: NR= Not Reported, N/A= Review article
S0376-6357(16)30358-8 http://dx.doi.org/doi:10.1016/j.beproc.2016.11.008 BEPROC 3332
To appear in:
Behavioural Processes
Received date: Revised date: Accepted date:
21-6-2016 13-11-2016 17-11-2016
Please cite this article as: Cussen, Victoria A., Psittacine Cognition: Individual Differences and Sources of Variation.Behavioural Processes http://dx.doi.org/10.1016/j.beproc.2016.11.008 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Psittacine Cognition: Individual Differences and Sources of Variation.
VICTORIA A. CUSSEN Department of Neurobiology, Physiology & Behavior, University of California, Davis
Correspondence: V.A. Cussen, Department of Neurobiology, Physiology & Behavior, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA (email: [email protected]; tel +1 (530) 752-0203; fax +1 (530) 752-5582.
Highlights
Psittacine cognition research originally focused on ‘proof of capacity’
Three species account for approximately half of all parrot cognition research
The number of psittacine species and individuals tested is expanding
Intraspecific variation is common in psittacine cognition research
Non cognitive factors such as personality may play a role in variation and should be controlled for in study design
Cognitive normal ranges need to be established for each species and assay
Abstract Both the number and breadth of avian cognition studies have expanded in the past three decades. Parrots have a long history as subjects in avian cognition research. This paper summarizes results from a number of parrot species tested on basic learning, and physical & social cognitive processes, with an emphasis on individual differences. Early psittacine studies were aimed at demonstrating a particular cognitive ability existed in a given species. Because of this proof of capacity focus, early studies typically included only a single individual or a dyad of parrots. Existing reviews of parrot cognition tend to focus on a particular cognitive component in a single species, or even a single individual. Despite the narrow focus, results from increasing sample sizes show intraspecific variation across a variety of cognitive assessments and parrot species. Intraspecific variability in performance on cognitive tasks highlights the need for establishing a cognitive normal range for a given species and process. To accomplish this, large numbers of individuals need to be tested and non-cognitive sources of variability need to be controlled. Once species typical cognitive normal ranges are established, cognitive comparisons can be made between parrot species and between parrots and other taxa.
Keywords: parrot; avian cognition; personality; individual differences; cognitive normal range
Introduction Birds have long been a staple of cognition research (e.g. Gossette et al. 1966), with the past three decades seeing an expansion in both the number and breadth of avian cognition studies (Willemet 2013). Fields of inquiry such as cognitive ecology are posing new questions about the adaptive function (Dukas 2004, Lefebvre et al. 2004, Morand-Ferron et al. 2015), fitness benefits (Boogert et al. 2011, Morand-Ferron et al. 2015, Sol et al. 2007) and possible trade offs (Healy 2012) of cognitive abilities. Research emphasis has shifted from generalized learning principles in pigeons to a broad range of cognitive processes across species (see reviews of episodic-like memory: Salwiczek, Wanatabe, and Clayton, 2010; navigation: McMillan et al. 2015; scatterhoarding: Pravosudov and Roth 2013; foraging: Healy and Hurly 2013; innovation: Griffin and Guez 2014).
Still, particular taxa remain more heavily represented in the literature than others. The Corviade family is an example. Since the string pull test pioneered by Bernd Heinrich (1995), corvids have been tested on a variety of social, physical, and general cognitive processes. Episodic-like memory (scrub jays, Clayton and Dickinson 1998), insightful tool use (New Celedonian crows, Taylor et al. 2011, but see Seed and Boogert 2012), and social cognition (ravens, Bugnyar 2011; 2013) are well documented (for reviews see Emery and Clayton 2004, Taylor 2014). The brains of some corvid species have enlargements in areas involved in higher order cognitive processes (relative to overall brain size, referred to as ‘relative brain size’, Iwaniuk et al. 2005). These brain areas are though to function in a similar way to the primate neocortex, providing the neural
substrate for advanced cognitive abilities (Reiner 2005, Jarvis et al. 2005, Güntürkün 2012). Parrots, like corvids, possess a large relative brain size that is equivalent to that of some primate species (Iwaniuk and Hurd 2005) and parrots are similarly regarded as cognitively sophisticated (Emery 2006). The parallel interest in corvid and psittacine physical cognition recently led to a direct comparison between those taxa (Auersperg et al. 2011).
Parrots have a long history as subjects in avian cognition research, at least partly due to Irene Pepperberg’s pioneering work with Alex the African grey parrot (see below). Early psittacine cognition research was characterized by ‘power studies,’ aimed at demonstrating a particular ability existed in a given species (Pepperberg and Funk 1990). In other words, a single individual exhibiting a given cognitive ability provided evidence that the capacity existed within that species - regardless of whether or not it was widespread. Because of this proof of capacity focus, early studies typically included only a single individual or a dyad of parrots. Unlike corvids, where reviews exist that span cognitive processes and/or species, reviews of parrot cognition tend to focus on a particular cognitive component in a single species, or even a single individual.
Finally, across taxa authors are beginning to explicitly examine individual variation and report the magnitude of that variation on experimental tasks (e.g. Guillette et al. 2011, 2015, Croston et al. 2016). Characterizing the cognitive abilities of a species requires developing a cognitive normal range. In much the same way that there are normal ranges for phenotypic parameters such as height, longevity, or heart rate in a species, the
cognitive normal range is the species-typical magnitude of between-subjects variation on a given cognitive process. Sample sizes in psittacine cognition studies have increased across time, providing descriptive information on intraspecific variation in task performance. However, individual differences have yet to be systematically investigated in parrot species.
This paper considers three decades of psittacine cognition research and summarizes the distribution of parrot species and individuals investigated, intraspecific differences reported, and possible causes of variation in test performance.
Psittacine Cognition Research Perhaps no individual bird is as emblematic of avian cognition research as Alex the African grey (Psittacus erithracus) parrot. Alex’s career as Irene Pepperberg’s test subject spanned three decades; their partnership is chronicled in the popular press book, The Alex Studies (Pepperberg 1999). Pepperberg’s work with Alex is summarized in multiple review articles: studies covered the development of basic cognitive processes using Piagetian stages (reviewed in Pepperberg 2002), referential learning and abstract category formation (reviewed in Pepperberg 2013), and numerical competence (reviewed in Pepperberg 2006a). Those early studies helped to catalyze interest in and expand understanding of psittacine cognition.
Subsequent research efforts have expanded the types of cognitive processes examined (e.g. Pepperberg 2004), the number of individual subjects included (e.g. Giret et al.
2010), and the parrot species studied (e.g. Brown and Magat 2011a). Table 1 lists 71 psittacine cognition studies, including species, sample size, cognitive process investigated. The studies listed cover 29 species of parrots. African grey parrots dominated early papers: 12 of 20 papers published prior to 2005 used African greys as their subjects, compared to a quarter of the 51 studies published after 2005. Both kea (Nestor notabilis) and orange-winged Amazon parrots (Amazona amazonica) have surpassed African greys as the most common study species. Psittacine cognition research programs now exist in Australia, Europe, South America, and the United States. Work done with wild and captive keas at the Konrad Lorenz Institute is an example of research assessing cognitive processes in a novel study species. The group has investigated innovation, social learning, tool use, and causal reasoning on a variety of tasks (for a review of research on ‘technical intelligence’ in keas, see Huber and Gajdon 2006).
Variation in Psittacine Cognition Since the late 1990s parrot cognition study sample sizes have generally increased, although the number of subjects remains highly variable across studies (see sample sizes in Table 1). Results from studies with larger sample sizes indicate that while a particular cognitive capacity may exist somewhere within a parrot species, it is not necessarily widespread (Schuck-Paim et al. 2009). For example, a study of innovation in wild kea found only 5 of 36 individuals successfully foraged from closed garbage cans (an assessment of physical cognition), and even these lid-opening individuals failed to open the lids on approximately 90% of their attempts (Gajdon et al. 2006). Krasheninnikova (2013) found the number of string pull tasks on which individual Galah cockatoos
(Eolophus roseicapilla) met criteria ranged from 2 to 5 tasks across subjects. Further, individuals that did complete the task significantly differed in the technique they used (Krasheninnikova 2013). African greys parrots’ performance on inference by exclusion tasks also ranged widely between individuals, by over 30% in some task conditions (Mikolasch et al. 2011). Even captive-bred siblings,vary in their performance on cognition tests (Piagetian development tasks, yellow crowned parakeets [Cyanoramphus auriceps] see Funk and Matteson 2004).
Despite growing evidence of variation in cognitive abilities (Thornton and Lukas 2012) the mechanisms mediating avian intraspecific variation are currently unknown (Griffin and Guez 2014). One possible mechanism is related to how information processing. In mammals, information can be preferentially processed in one of the two cerebral hemispheres and the strength of the hemispheric dominance (‘cerebral lateralization’), is linked to cognitive function and behavioral performance (Rogers 1996). Similar processing asymmetries occur in avian brains, which lack hemispheres (Brown and Magat 2011b, Rogers 2009). Cerebral lateralization can be indirectly measured by motor lateralization, or limb preference. The strength of limb preference in parrots appears to be correlated with cognition. For example, more strongly lateralized birds performed better on both means end discrimination (Magat and Brown 2009) and spatial memory (Cussen and Mench 2014a) tasks. Those studies report both species differences and intraspecific variation in the strength of motor lateralization and cognitive performance. An important first step in understanding mechanisms of cognitive variability is to characterize the
species-typical cognitive normal range for a given task (e.g. Cole et al. 2012), and to determine how much of the variability is related to non-cognitive factors.
Non-Cognitive Contributors to Variability In addition to differences in cognitive ability, variation in results can be caused by noncognitive factors that influence individual task performance. Morrand-Ferron and colleagues (2015) identified the following four non-cognitive factors that could contribute to variability in cognition studies: perceptual and motor biases, motivation, personality, and environmental factors. For example, both keas (Miyata et al 2011) and orange-winged Amazons (Cussen and Mench 2014a) showed side biases when interacting with the test apparatus. Keas are neophilic and readily interact with novel objects (Huber and Gajdon 2006), but many other parrots species tend towards neophobia (e.g. African greys, Péron et al. 2011). The correlation between neophobia (a personality trait) and problem solving ability conflicts across studies (see review in Griffin and Guez, 2014). But individual differences in personality can influence cognition (e.g. susceptibility to attention biases, Cussen and Mench 2014b) and learning strategies (Mathieu et al. 2012), although much remains to be clarified about this relationship (Griffin et al. 2015). These and the other non-cognitive factors discussed below are important variables to quantify and/or control when designing or interpreting psittacine cognition research. Otherwise, incorrect inferences can be drawn about a species cognitive normal range or about interspecific comparative cognition.
Testing Environment: Krasheninnikova and Schneider (2014) tested orange-winged Amazons on a series of seven string pull tasks. Some parrots were tested individually and others were allowed to interact with the task in a social condition. Parrots in the social condition had a higher participation rate and the majority of subjects completed all string pull tasks. Only half of the individually tested parrots completed all tasks. It is possible that testing parrots in social settings reduces neophobia when interacting with a novel task and contributes to success (though stimulus enhancement may play a role, e.g. Mikolasch et al 2012). Either way, the social environment during cognitive tests can influence parrots’ success.
Conspecific influence can also depend on the identity of the social group members. African grey parrots chose to interact with a cooperative string pull apparatus preferentially depending on the identity of the available partner (Péron et al. 2011) and reciprocity was influenced by dominance rank of the individual being tested (Péron et al. 2013). Dominance rank also played an important role in a cooperation task given to keas, with dominant individuals able to monopolize the reward and coerce subordinates to assist with the task (Tebbich et al 1996).
Sex Differences: Sex can contribute to variability in test results (Healy et al. 2009) but sex differences remain largely unexplored in parrots, likely because of small sample sizes. While no female keas were successful in opening garbage lids (Gajdon et al. 2006), only of a minority of males were successful and the overall low success rate makes sex comparisons difficult. Krasheninnikova and Wanker (2010) directly tested for sex effects
and found no difference on a string pull task in spectacled parrotlets (Forpus conspicillatus). Many studies had too few subjects, or subjects of unspecified sex, to test for sex effects directly (see sex ratio in Table 1).
Subject History: Unlike work in other taxa (e.g. Pravosudov and Roth 2013), psittacine cognition research is dominated by comparative cognition approaches in captive settings. This may reflect the complex testing paradigms, which can require extensive training and lend themselves well to laboratory studies (Giret et al. 2010), or may result from the general difficulty of assaying cognition in the field (Morand-Ferron et al. 2015). Wild, free-living parrots were subjects in 7 of the 71 studies indexed in Table 1, with one other study using wild caught, captive subjects. A further 15 of the 71 studies included subjects with a mixture of backgrounds (wild caught and captive bred), and several more included captive bred parrots that were either parent- or hand- reared (4 and 18 studies of 71, respectively). The majority of studies (n=26) used captive subjects whose backgrounds were either unknown or unreported (see Status in Table 1). Early life experience is known to have significant effects on parrot development (Fox and Millam, 2004), making subject background an important variable to report and to consider in analyses.
The effect of subject history is evident in differential performance between laboratoryreared and wild conspecifics, a phenomenon that is documented in several species (Huber and Gajdon 2006) from cognitive tasks to physiological parameters (e.g. Calisi and Bentley 2009). For example, captive kea tested on a physical cognition assay readily learned the required task; the majority of the kea solved it spontaneously and the
remaining birds learned the solution after it was demonstrated to them. However, only 3 of 21 color banded wild keas learned how to solve the same task, and then only after the experimenters trained a demonstrator bird (Gajdon et al. 2004). Variability in backgrounds is sometimes unavoidable, such as in zoo studies, but it is an important variable to consider when interpreting results, as life experience may confound the results of between species or subjects comparisons.
Inhibition of Response: Finally, several authors have raised the issue of impulsivity in parrots (e.g. de Mendonça-Furtado and Ottoni 2008, but see Koepke et al. 2015). The apparent inability to inhibit motor control was thought to impair performance on cognitive tests in several studies (Cussen and Mench 2014a, Péron et al 2011, Mikolasch et al. 2012). Explicitly testing inhibitory control across parrot species could aid in interpretation of results in the future (Liedtke et al. 2011).
Conclusion The large Psittacidae family (over 400 species, Joseph et al. 2004) is well suited to phylogenetic studies of cognitive abilities (Mettke-Hoffman et al. 2002) and mechanisms underpinning cognitive variability (Mettke-Hoffman 2014) . Still, the vast majority of studies, with a few notable exceptions (e.g. Auersperg et al. 2014, Brown and Magat 2011a, Magat and Brown 2009), involve a single parrot species. Psittacine cognition research generally is limited to African grey parrots, kea, and orange-winged Amazon parrots. Those three species account for almost half of the parrot subjects listed in Table 1. In addition to increasing the number of species investigated, testing should be carried
out in both the wild, where normal ecological and developmental conditions occur, and in the laboratory, where non-cognitive factors can be better controlled (Rowe and Healy 2014, Sulikowski and Burke 2015, Brown & Magat 2011a) Newly available automated operant devices can be used to test cognitive processes in free-living individuals (e.g. Morand Ferrond et al. 2013). Identifying and controlling non-cognitive factors such as rearing history, sex, age, previous testing experience, etc. (for an example, see Auersperg et al. 2015) will allow for partitioning of variance that does not reflect variation in cognitive ability.
In 30 years of research effort, 462 unique individual parrots (28 African greys, 55 orangewinged Amazons, and 128 keas) were used as subjects in cognition research.. Birds of a given species vary in ways that have important consequences for their behavior and overall fitness (Dingemanse and Wolf 2010, Smith and Blumstein 2008) from physiological differences (Koolhaas et al. 2010) to differences in behavior (van Oers et al. 2005) and decision-making (Morgan et al. 2014). The shallow subject pool hampers understanding of the distribution and adaptive value of cognitive processes within parrot species. Determining a cognitive normal range, or the intraspecific variability on a particular cognitive task, requires testing large numbers of individuals (e.g. Cole et al., 2011). Focusing research effort on the three commonly-studied parrot species (African grey, kea and orange-winged Amazons) and selecting cognitive tasks that have existing data from the largest number of unique individuals would be a good starting point for expanding the number of subjects tested in support of developing cognitive normal
ranges for those tasks. Then these ranges can be used to make meaningful comparisons between parrot species, and between psittacines and other avian taxa. Acknowledgments I am grateful to Professor Thomas Coombs-Hahn for providing support while writing this manuscript. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Table Table 1: Psittacine cognition articles. A variety of cognitive processes have been studies, mainly in African grey, Kea, and orange-winged Amazon parrots. Sample sizes have generally increased over the years, but remain highly variable and often small. BASIC PROCESSES: Status* Sex Sample Assessment Author Species M:F** (n) Giret et al. African grey (Psittacus 4 1:1 2 Categorization (2009a) erithacus) Referential label Giret et al. 6 NR 10 learning (2010) African grey Inference by Mikolasch et al. 5 4:3 7 exclusion (2011) African grey Local Mikolasch et al. 5 4:3 7 enhancement (2012) African grey Delay of 4 2:1 3 gratification Vick (2010) African grey Category Pepperberg 5 1:0 1 comprehension (1990) African grey Conjunctive label Pepperberg 5 1:0 1 comprehension (1992) African grey Category Pepperberg 5 1:0 1 comprehension (2013) African grey Delay of Koepke et al. 4 1:0 1 gratification (2015) African grey Piagetian Pepperberg et 4 1:0 1 development al. (1997) African grey African grey, Illiger macaw (Ara maracana), Cockatiel (Nymphicus hollandicus), Parakeet (Melopsittacus undulates)
Blue fronted Amazon
N/A Orange-winged Amazon (Amazona amazonica)
5
5
N/A 3
N/A
4
Object permanence
N/A
Learning set generalization Piagetian Framework Review
5:8
Cognitive bias (attention bias)
1:0
1
12
Pepperberg and Funk (1990) de MendonçaFurtado and Ottoni (2008) Pepperberg (2002) Cussen and Mench (2014b)
Orange-winged Amazon Orange-winged Amazon Rainbow lorikeet (Trichoglossus moluccanus) Yellow-crowned parakeet (Cyanoramphus auriceps) Yellow-crowned parakeet Yellow-headed Amazon (Amazona oratrix)
3
5:8
12
5
1:1
2
Learning set acquisition & breaking, long term memory Analogical reasoning
12
Win-shift/winstay strategy
5
NR
6
7:4
11
6
NR
11
Piagetian development Piagetian development Discrimination & reversal learning Foot preference & lexicon size Laterality of foot use Knowledge transfer Means-end comprehension Discrimination discrete & continuous amounts Inferential reasoning
2
NR
2
African Grey
5
NR
524
23 Australian species
6
NR
1
Kea (Nestor notabilis)
5
5:1
6
8 Australian Species
5
NR
40
African Grey
4
2:1
3
African Grey
6
3:1
4
Status
Sex M:F
African Grey
4
2:0
2
African Grey
5
3:3
6
African Grey
5
1:0
1
Mirror tasks Inferential reasoning Numerical competence
African Grey
5
1:0
1
Zero-like concept
Cussen and Mench (2014a) Obozova et al. (2015) Sulikowski and Burke (2011) Funk and Matteson (2004) Funk (1996) Gossette et al. (1966) Synder and Harris (1997) Brown & Magat (2011a) Gajdon et al. (2013) Magat and Brown (2009)
Aïn et al. (2009) Pepperberg et al. (2013)
PHYSICAL COGNITION: Species
Sample Assessment (n)
Author Pepperberg et al. (1995) Schloegl et al. (2012) Pepperberg (2006) Pepperberg (2006)
Labels Means-end comprehension
Pepperberg (2006) Pepperberg (2012) Pepperberg (1994) Pepperberg and Brezinsky (1991) Pepperberg and Gordon (2005) Pepperberg and Shive (2001) Pepperberg (2004)
61
Play
Auersperg et al. (2014)
16
Means-end comprehension
Krasheninnikova (2013)
Auersperg et al. (2015)
African grey
5
1:0
1
African Grey -
5
1:0
1
African Grey
5
1:0
1
African Grey
5
1:0
1
African Grey
5
1:0
1
African Grey
4
1:0
1
African Grey Black palm cockatoo (Probosciger aterrimus), Kea; African grey, Black billed Amazon (Amazona agilis), Yellow billed Amazon (Amazona collaria), Goffin cockatoo (Cacatua goffiniana) Galah cockatoo (Eolophus roseicapilla), Cockateil Goffin cockatoo, Red shouldered macaw (Diopsittaca nobilis), Black headed caique (Pionites melanocephalus) Hyacinth (Anodorhynchus hyacinthinus) and Lear's macaw (Anodorhynchus leari), Blue-fronted Amazon (Amazona aestiva)
6
4:0
4
6 3
NR NR
Numerical competence Numerical competence Quantity discrimination Class concept Numerical competence
4
NR
22
Play
6
8:10
10
Means-end comprehension
Hyacinth Macaws
6
2:4
6
Tool use
Kea
6
6:0
6
Kea
N/A
N/A
12
Tool use Technical intelligence
Schuck-Paim et al. (2009) Borsari and Ottoni (2005) Auersperg et al. (2011) Huber and Gajdon (2006)
Review Kea
6
7:0
10
Kea
6
1:0
10
Kea
4
5:2
7
Artificial fruit Inference by exclusion Means-end comprehension
Kea, Macaw, Cockatoo
5
NR
10
Trap tube
58
Means-end comprehension
Orange-winged Amazon
PHYSICAL COGNITION: Species (cont’d) Spectacled parrotlet, Rainbow lorikeet, Green-winged macaw (Ara chloroptera), Sulphur crested cockatoo (Cacatua galerita) Yellow-crowned Parakeet
5
NR
Status
Sex M:F
5
NR
39
6
NR
11
Status
Sex M:F
Sample Assessment (n)
Means-end comprehension Means-end comprehension
Miyata et al. (2011) Schloegl et al. (2009) Werdenich and Huber (2006) Liedtke et al. (2011) Krasheninnikova and Schneider (2014) Author
Krasheninnikova et al. (2013) Funk (2002)
SOCIAL COGNITION: Species African Grey
5
0:1
African Grey
4
2:1
African Grey
4
2:1
African Grey
4
2:0
African Grey
4
2:0
African Grey
4
2:0
Sample Cognitive (n) Process Social context & vocalizations Discrimination of 3 vocalizations Use of experimenter 3 given cues Vocal learning – 2 social impact Reciprocity & 2 sharing Acquisition of human language 2 labels
Author Colbert-White et al. (2011) Giret et al. (2009b) Giret et al. (2009c) Pepperberg et al. (1999) Péron et al. (2013) Pepperberg and McLaughlin (1996)
African Grey
4
2:1
3
African Grey
4
1:0
1
African Grey
4
1:0
1
African Grey Crimson rosella (Platycercus elegans)
6
3:0
3
1
NR
182
Cooperation Vocal learning – social impact Reciprocity & sharing Acquisition of human language labels
Green-rumped parrotlet (Forpus passerinus)
1
NR
34
N/A Social transmission tool manufacture Social transmission unique calls
Kea
5
5:7
1
Social learning
Kea
1
23:12
36
Social learning
Kea
6
5:2
7
Cooperation
Goffin cockatoo
4
6:6
12
Péron et al. (2011) Pepperberg et al. (2000) Péron et al. (2014) Pepperberg and Wilcox (2000) Ribot et al. (2012) Auersperg et al. (2014b) Berg et al. (2011) Huber et al. (2001) Gajdon et al. (2006) Tebbich et al. (1996) Gajdon et al. (2004) Moura et al. (2014)
1 NR 21 Social learning Kea Gestural Orange-winged 1 8:8 32 communication Amazon Yellow-naped Parrot Dahlin and (Amazona 1 1:1 38 Syntax in duets Wright (2012) auropalliata) *Status: 1=Free-living, 2=Captive: Wild caught, 3=Captive Bred: Parent reared, 4=Captive Bred: Hand reared, 5=Captive: Breading & rearing unknown/unspecified, 6=Captive: Mixed backgrounds **Sex: NR= Not Reported, N/A= Review article