Article Tracking Changes of Hidden Food: Spatial Pattern Learning in Two

Pizza Ka Yee Chow 1,2,*,† , James R. Davies 1,2,3,† , Awani Bapat 1,2,4 and Auguste M. P. von Bayern 1,2

1 Max Planck Institute for Ornithology, Eberhard-Gwinner-Straße, 82319 Seewiesen, Germany; [email protected] (J.R.D.); [email protected] (A.B.); [email protected] (A.M.P.v.B.) 2 Max-Planck Comparative Cognition Research Station, Fundación, 38400 Puerto de la Cruz, , 3 Comparative Cognition Lab, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, UK 4 Department of Behavioral and Cognitive Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria * Correspondence: [email protected] † Share first authorship.

Simple Summary: Efficiency in locating available food sources, which vary spatially and temporally, using spatial distribution patterns may differ depending on a species’ diet and habitat specialisation. We hypothesised that more generalist species would acquire spatial information faster than more specialist species, due to being more explorative when changes occur. We tested this hypothesis by presenting a ‘poke box’ to relatively more generalist Great Green and relatively more specialist Blue-throated Macaws. The ‘poke box’ contained hidden food placed within wells that formed two patterns. The two patterns changed on a mid-week schedule. We found that (1) the two patterns varied in their difficulty; and (2) the more generalist Great Green Macaws took fewer trials to   learn the easier pattern and made more mean correct responses in the difficult pattern, than the more specialist Blue-throated Macaws, thus supporting our hypothesis. The Great Green Macaws’ better Citation: Chow, P.K.Y.; Davies, J.R.; learning performance may be explained by more exploration and prioritising accuracy over speed. Bapat, A.; von Bayern, A.M.P. These results suggest how variation in diet and habitat specialisation may relate to a species’ ability Tracking Changes of Hidden Food: Spatial Pattern Learning in Two to adapt to spatial changes of food resources, which will be useful for the conservation efforts for the Macaw Species. 2021, 2, 285–301. two critically endangered species to understand their abilities to cope with environmental change. https://doi.org/10.3390/ birds2030021 Abstract: Food availability may vary spatially and temporally within an environment. Efficiency in locating alternative food sources using spatial information (e.g., distribution patterns) may vary Academic Editor: Jukka Jokimäki according to a species’ diet and habitat specialisation. Hypothetically, more generalist species would learn faster than more specialist species due to being more explorative when changes occur. We tested Received: 30 June 2021 this hypothesis in two closely related macaw species, differing in their degree of diet and habitat Accepted: 4 August 2021 specialisation; the more generalist and the more specialist Blue-throated Macaw. Published: 9 August 2021 We examined their spatial pattern learning performance under predictable temporal and spatial change, using a ‘poke box’ that contained hidden food placed within wells. Each week, the rewarded Publisher’s Note: MDPI stays neutral wells formed two patterns (A and B), which were changed on a mid-week schedule. We found with regard to jurisdictional claims in that the two patterns varied in their difficulty. We also found that the more generalist Great Green published maps and institutional affil- Macaws took fewer trials to learn the easier pattern and made more mean correct responses in the iations. difficult pattern than the more specialist Blue-throated Macaws, thus supporting our hypothesis. The better learning performance of the Great Green Macaws may be explained by more exploration and trading-off accuracy for speed. These results suggest how variation in diet and habitat specialisation may relate to a species’ ability to adapt to spatial variation in food availability. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Keywords: ; ambiguus; Ara glaucogularis; memory; foraging; generalist; specialist; compar- This article is an open access article distributed under the terms and ative cognition conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

Birds 2021, 2, 285–301. https://doi.org/10.3390/birds2030021 https://www.mdpi.com/journal/birds Birds 2021, 2 286

1. Introduction Many species encounter spatial and temporal fluctuations of food availability in their natural environment. When food becomes temporarily unavailable at a location, behavioural flexibility is required to locate alternative food sources in order to survive. To deal with the variability in the environment, foragers may utilise spatial (e.g., distribution patterns) and specific (e.g., visual cues) environmental information to increase foraging efficiency [1–4]. The extent to which a species may use this information to locate food resources, may depend on ecological factors such as diet and habitat specialisation. For example, species that are more specialised in diet have been shown to pay more attention to specific information than generalists [5]. Being more sensitive to specific or relevant information may allow specialists to excel at manipulating certain food types efficiently in stable environments [6,7], or when encountering different but similar problems [8]. While more generalist species have been found to be slower at making decisions than specialists [9], they appear to be characterised by showing more exploratory behaviour [10] and explorative foraging techniques [11]. This may allow them to adapt to changes faster than more specialist species [12]. However, the role of ecological factors such as diet and habitat specialisation, in relation to a species’ aptitude in acquiring environmental information when food distributions change, remains unclear. The aim of this study is to examine the role of diet and habitat specialisation in relation to acquiring predictably changing spatial information. To do this, we adapted one of the well-established spatial pattern learning paradigms, which require individuals to search for hidden food (e.g., in matrices of poles, wells or on checkboards) that vary spatially and temporally e.g., [13–16]. We also examined how individuals acquired spatial information in such a situation (e.g., examining their behaviour in relation to exploration and speed-accuracy trade-offs). We compared spatial learning performance in two closely related macaw species, considered to vary in their diet and habitat specialisation: Great Green Macaws (Ara ambiguus) (hereafter, GG) and Blue-throated Macaws (A. glaucogularis) (hereafter, BT). Investigation into their ability and speed in utilising environmental information to locate food sources, and in particular when a change occurs, will be useful for the conservation efforts of the two critically endangered species (GG: [17,18]; BT: [19,20]) to understand their ability in adapting to ecological change. Both species live in fairly stable social groups and are often observed foraging in flocks (BT: [21]; GG: [22]). As documentation of the full diet habits of both species in the wild is limited, especially BT, Levin’s niche breadth [23] to calculate the relative diet generalisation of each species is currently unavailable. However, available records appear to indicate that GG adapt to a wider variety of habitats, which vary in their seasonality, than BT, suggesting that GG may exploit a greater variety of foods than BT. For example, GG inhabit seasonally dry forests on the southern Pacific coast of , as well as less seasonal wet tropical forests from to [22,24,25], whereas BT (historically and currently) only inhabit seasonal savannah habitats in relatively restricted areas of Beni, Bolivia [21]. Here, the main food source of BT, motacú palms (Attalea phalerata), produce continuously throughout the year [26]. This suggests that the need to explore alternative food sources (and thus food variety) for BT may be lower than GG. Importantly, although BT show flexibility in utilising alternative resources during nesting [27], as well as occasionally consuming other foods such as , nuts, and flowers (which GG also do) [28,29], they appear to be more specialised in diet than GG. BT consume more than seeds [21,26,30,31] and not only do they rely on the presence of motacú palms to survive, but their alternative food sources also appear to be other species of palms (e.g., Acrocomia aculeata, and Mauritia fleuxosa)[21,26,30,31]. In contrast, GG feed more on seeds and nuts than fruit [22], and despite showing a preference for feeding in almendro trees (Dipteryx oleifera) and beach almond trees ( catappa) during their respective fruiting seasons, they otherwise feed on a wide variety of species, such as titor trees (e.g., Sacoglottis trichogyna), and quaruba (e.g., Vochysia ferruginea), to name a Birds 2021, 2 287

few (see food list in Humedal Maquenque Anexo #2, also see [22,25,32–34]. Such variation in diet composition between the two species may also be related to differing energetic requirements in relation to their body size [28]. Nevertheless, the discussed differences in ecologies suggest that the two species are suitable for us to examine our hypothesis: that variation in diet and habitat specialisation would affect a species’ speed in acquiring spatial information. Specifically, we predicted that in a test situation featuring constant and predictable recurring temporal change, the more generalist GG would be more explorative and show better spatial pattern learning performance than the more specialist BT. We additionally examined their learning strategies to understand how individuals process spatial information.

2. Methods 2.1. Study Species and Housing Six individuals from each species (Table1) participated in this study between August 2019 and March 2020. These macaws were hand-raised by the Loro Parque Foundation in Tenerife (Spain) and were group-housed, by species, in 5 connected semi-outdoor aviaries at the Comparative Cognition Research Station situated in Loro Parque, Puerto de la Cruz, Tenerife (Note S1). The parrots received natural light and ambient outdoor temperature at the back part of each aviary. Arcadia Bars (Arcadia 54 W Freshwater Pro and Arcadia 54 W D3 Reptile lamp) were installed at the front of the aviary to ensure the parrots received sufficient exposure to UV light. This experiment did not involve any invasive methods, negative reinforcement, or punishment. The parrots were fed twice a day with fresh fruit, seeds, and vegetables. Additional high-quality food rewards (nut pieces) could be obtained during the experiment. Water was accessible ad libitum at all times. We provided enrichment and monitored the parrots’ health at least twice per week.

Table 1. Individual characteristics (name, age, sex, and mean weight in grams) for each species. Note that the mean weight is the average of the weights taken during the regular health checks over the study period (August 2019 to March 2020).

Great Green Macaws Blue-Throated Macaws (Ara ambiguus) (A. glaucogularis) Name Age Sex Weight (g) Name Age Sex Weight (g) Hagrid 5 M 1213 Mowgli 5 M 762 Enya 5 F 1160 Charlie 5 M 783 Luna 5 F 1129 Long John 6 M 746 Madame 5 F 1064 Gargamel 7 M 849 Alba 5 F 1153 Lady 5 F 728 Rita 5 F 1119 Mr. Huang 6 M 812

2.2. Test Room Set Up Inside the test room (Length × Width × Height: 1.5 × 1.5 × 1.5 m), one wall was light green and the opposite wall was white. There was a sound-buffered, one-way glass panel connecting the two walls, which allowed zoo visitors to observe the experiments live (Figure1A). Three tables (each 87 × 49 × 150 cm) were placed in the room, with the middle table being a sliding table. The experimental apparatus, i.e., the ‘poke box’ (see below) was attached to the centre of another white table that was placed on top of the sliding table, so that it could be moved forward to be replenished with food rewards during inter-trial intervals. The sliding table was marked by three strips of black tape: two thin strips running parallel along the outer sides of the poke box facing the walls, and a third thick strip running perpendicular to the others and underneath the poke box (Figure1A ). We used two (out of four) surveillance cameras, in the top corner and side positions of the test room, to observe and record the behaviour of the parrots. The test room had additional visual elements that consisted of electric heaters, lights, and ventilation fixtures. These provided unique spatial features relative to the poke box at the centre of the room, which Birds 2021, 2, FOR PEER REVIEW 4

table, so that it could be moved forward to be replenished with food rewards during inter- trial intervals. The sliding table was marked by three strips of black tape: two thin strips running parallel along the outer sides of the poke box facing the walls, and a third thick strip running perpendicular to the others and underneath the poke box (Figure 1A). We used two (out of four) surveillance cameras, in the top corner and side positions of the test Birds 2021, 2 room, to observe and record the behaviour of the parrots. The test room had additional 288 visual elements that consisted of electric heaters, lights, and ventilation fixtures. These provided unique spatial features relative to the poke box at the centre of the room, which the parrots may use as ‘landmarks’. The lights were flicker-free and covered the parrots’ the parrots may use as ‘landmarks’. The lights were flicker-free and covered the parrots’ full range of visible light (Arcadia 39 W Freshwater Pro and Arcadia 39 W D3 Reptile full range of visible light (Arcadia 39 W Freshwater Pro and Arcadia 39 W D3 Reptile lamp). lamp).

Figure 1. PokeFigure box set1. Poke up for box testing set up the for macaws’ testing the spatial macaws’ learning spatial performance. learning performance. (A) The set up (A in) The the testset up room; in (B) base the test room; (B) base wooden layer with 12 wells filled with inaccessible food (seeds for habitua- wooden layer with 12 wells filled with inaccessible food (seeds for habituation and nut pieces for training); (C) the divider tion and nut pieces for training); (C) the divider with holes used to separate the top and the bottom with holes used to separate the top and the bottom layers with holes to release scent; (D) the upper wooden layer containing layers with holes to release scent; (D) the upper wooden layer containing the accessible rewards the accessible(seeds rewards or nuts); (seeds and or nuts);(E) the and top ( plexiglassE) the top plexiglasslayer with layerpaper with covering paper the covering wells. the wells.

2.3. Experimental2.3. Apparatus Experimental Apparatus To examine theTo parrots’ examine spatial the parrots’ learning spatial performance, learning performance,the ‘poke box’ the design ‘poke was box’ design was adapted from adapted[35,36]. It from was [a35 flat,36 square]. It was box a flat (30.5 square × 30 × box 3.7 (30.5cm; Figure× 30 × 1A)3.7 containing cm; Figure 121A) containing wells (each 6 cm12 wellsdiameter) (each spaced 6 cm diameter) equally in spaced a 3 × 4 equallymanner. in The a 3 box× 4 (from manner. bottom The to box top) (from bottom to consisted of fourtop) major consisted parts: of (1) four the major bottom parts: consisted (1) the of bottom two wooden consisted layers of two(each wooden 30.5 × layers (each 30 × 1 cm) (hereafter,30.5 × 30the× bottom).1 cm) (hereafter, Each well the in this bottom). bottom Each part well was in filled this with bottom chopped- part was filled with up nuts whichchopped-up were inaccessible nuts which (Figure were 1B) inaccessible but released (Figure a scent.1B) (2) but A releasedwhite Plexiglas a scent. (2) A white sheet (0.2 mmPlexiglas thick) that sheet had (0.212 sets mm of thick) five holes that (each had 12 0.2 sets mm of diameter) five holes in (each clusters 0.2 cor- mm diameter) in responding toclusters the wells corresponding in the bottom; to this the wellsallowed in the the bottom; scent of this the allowed nuts to thepass scent through of the nuts to pass to the top wellsthrough (Figure to 1C), the topthus wells serving (Figure as a1 controlC), thus for serving the use as aof control olfactory for cues the use in this of olfactory cues × × task. (3) The topin thispart task. consisted (3) The of topanother part consistedwooden layer of another (30.5 × wooden 30 × 1 cm) layer onto (30.5 which30 a 1 cm) onto which a white Plexiglas sheet (0.5 mm thick) was placed (hereafter, the top). The wells in white Plexiglas sheet (0.5 mm thick) was placed (hereafter, the top). The wells in this part this part contained accessible rewards (Figure1D). (4) White paper was placed under the contained accessible rewards (Figure 1D). (4) White paper was placed under the top Plex- top Plexiglas sheet to cover the rewards (Figure1E), and thus blocking visual access to iglas sheet to cover the rewards (Figure 1E), and thus blocking visual access to the rewards the rewards in the wells (Figure1E). The whole box was then placed in the middle of the in the wells (Figure 1E). The whole box was then placed in the middle of the table in the table in the test room, secured with metal screws and brackets on each side attached to a test room, secured with metal screws and brackets on each side attached to a wooden wooden board (40 × 40 × 0.8 cm), fixed to the table. board (40 × 40 × 0.8 cm), fixed to the table. 2.4. Procedures Each was tested individually and had been previously trained to voluntarily enter a transporting cage (1.5 × 1 × 1.5 m; Figure2A). This transporting cage had a sliding board on one side that could be pulled up to separate a from the main aviary and move it to the test room. The cage was then parked next to a wooden window integrated into the door of the test room (0.5 × 0.5 m; Figure2A). Once the sliding board was lowered, the parrot entered the test room via a wooden ladder (Figure2B).

Birds 2021, 2, FOR PEER REVIEW 5

2.4. Procedures Each bird was tested individually and had been previously trained to voluntarily enter a transporting cage (1.5 × 1 × 1.5 m; Figure 2A). This transporting cage had a sliding board on one side that could be pulled up to separate a parrot from the main aviary and Birds 2021, 2 move it to the test room. The cage was then parked next to a wooden window integrated289 into the door of the test room (0.5 × 0.5 m; Figure 2A). Once the sliding board was lowered, the parrot entered the test room via a wooden ladder (Figure 2B).

FigureFigure 2. 2. ((AA)) Mowgli, Mowgli, a Blue-throatedBlue-throated Macaw,Macaw, in in the the transporting transporting cage cage parked parked next next to theto the door door of theof the test room, with the sliding board of the transporting cage lowered down. The door has a window test room, with the sliding board of the transporting cage lowered down. The door has a window adjacent to the cage, in which the macaw can enter the test room. (B) A screenshot taken from the adjacent to the cage, in which the macaw can enter the test room. (B) A screenshot taken from the test room surveillance camera, showing Madame, a Great Green Macaw, completing a trial. test room surveillance camera, showing Madame, a Great Green Macaw, completing a trial. The parrots were first habituated to the box and trained to obtain food (seeds) from The parrots were first habituated to the box and trained to obtain food (seeds) from the wells by tearing paper (Note S2). The main training started once a parrot tore the pa- the wells by tearing paper (Note S2). The main training started once a parrot tore the per, using its beak, of 10 (out of 12) or more wells for two or more consecutive days. As paper, using its beak, of 10 (out of 12) or more wells for two or more consecutive days. As the parrots appeared to struggle to tear dry paper, we applied a ring of water over each the parrots appeared to struggle to tear dry paper, we applied a ring of water over each wellwell in in a a standardised standardised manner manner to to facilitate facilitate tearing tearing (but (but ensured ensured that tearing tearing the paper paper still requiredrequired effort), effort), after after the the box box was was set set up up (Figure 11E).E). InIn thethe trainingtraining phase,phase, twotwo spatialspatial patternspatterns of of rewarded rewarded wells wells (A (A and B; Figure 33)) werewere created.created. PatternPattern AA consistedconsisted ofof thethe twotwo columns columns at at the the outer outer edges edges of of the the box box (6 (6 wells), whereas whereas pattern pattern B B consisted of of the two middle columns of the box (6 wells). The parrots experienced three trials of each pattern for three consecutive days (see below for further information). The pattern was then switched for the next 3 days of the week, with no testing on the last day of the week. We counterbalanced the pattern that individuals experienced first, within each species. The order of presenting the patterns was fixed for each individual across the training weeks. Birds 2021, 2, FOR PEER REVIEW 6

two middle columns of the box (6 wells). The parrots experienced three trials of each pat- tern for three consecutive days (see below for further information). The pattern was then switched for the next 3 days of the week, with no testing on the last day of the week. We Birds 2021, 2 290 counterbalanced the pattern that individuals experienced first, within each species. The order of presenting the patterns was fixed for each individual across the training weeks.

Figure 3. The two spatial patterns (A,B) containing rewarded wells (represented in black) during the Figure 3. The two spatial patterns (A and B) containing rewarded wells (represented in black) dur- main training. The pattern (A) or (B) that an individual experienced first was counterbalanced within ing the main training. The pattern (A) or (B) that an individual experienced first was counterbal- ancedeach specieswithin each (i.e., species three parrots (i.e., three received parrots pattern received A first,pattern whereas A first, the whereas other the three other parrots three received parrots receivedpattern Bpattern first). TheB first). order The of presentingorder of presenting the patterns the was patterns fixed forwas each fixed individual for each acrossindividual the training across theweeks. training Each weeks. week, Each each parrotweek, experiencedeach parrot experien each patternced each for 3 pattern consecutive for 3 daysconsecutive (3 trials days per day) (3 trials with pera daybreak. day) with a daybreak.

BeforeBefore each each trial, trial, we we baited baited the the wells wells according according to the to pattern the pattern (A or (A B) orthat B) the that indi- the vidualindividual received received on that on day. that We day. cleaned We cleaned the top theof the top box of and the the box tables and thebefore tables each before trial started;each trial this started; minimised this additional minimised cues additional being provided cues being to the provided parrots to during the parrots training. during We loweredtraining. the We board lowered of the the transporting board of the cage transporting to initiate the cage start to initiateof each thetrial. start The of trial each ended trial. withThe trialthe parrot ended voluntarily with the parrot re-entering voluntarily the transporting re-entering cage. the transportingBetween trials, cage. we Betweenblocked visualtrials, access we blocked to the visual test box access by toclosing the test the box window by closing of the the test window room; of this the prevented test room; the this parrotsprevented from the directly parrots observing from directly the observinglocations of the the locations rewards. of Each the rewards. inter-trial Each interval inter-trial did notinterval last longer did not than last 2 longerminutes than during 2 min training during trials. training Once trials. the parrot Once entered the parrot the entered test room, the thetest experimenter room, the experimenter turned away turned (to avoid away uncons (to avoidcious unconscious cueing towards cueing the towards food locations) the food andlocations) recorded and its recorded choices itswhile choices directly while observing directly observingvia a smartphone via a smartphone connected connected to the sur- to veillancethe surveillance cameras cameras (Figure (Figure1B). We1B). repeated We repeated this procedure this procedure 3 times 3 times for each for eachsession. session. If a If a parrot reached ρ ≥ 80% (see below) on the second and third trial, we ran a fourth trial parrot reached ρ ≥ 80% (see below) on the second and third trial, we ran a fourth trial so so as to determine whether the individual reached the criterion (ρ ≥ 80% for 3 consecutive as to determine whether the individual reached the criterion (ρ ≥ 80% for 3 consecutive trials). We continued the experiment for 10 weeks, regardless of whether the parrots had trials). We continued the experiment for 10 weeks, regardless of whether the parrots had reached the criterion, to compare learning performance with increased experience. A third reached the criterion, to compare learning performance with increased experience. A third rater (AB) re-coded the order of choices from the available videos (2.5% of the videos were rater (AB) re-coded the order of choices from the available videos (2.5% of the videos were lost due to system errors and unforeseen circumstances e.g., vet visits) and obtained high lost due to system errors and unforeseen circumstances e.g., vet visits) and obtained high inter-rater reliability (ICC: BT = 0.999, GG = 0.999). inter-rater reliability (ICC: BT = 0.999, GG = 0.999). Behavioural Measurements Behavioural Measurements Learning performance. We considered a parrot to have learned a pattern if it reached rho (Learningρ) ≥ 0.8 performance. (or 80%) correct We considered (rewarded) a responses parrot to acrosshave learned three consecutive a pattern if trials.it reached This rhoρ value (ρ) ≥ is0.8 positively (or 80%) relatedcorrect (rewarded) to Mann–Whitney responses U test,across with three an emphasisconsecutive on trials. consecutive This ρ valuecorrect is responsespositively beingrelated made to Mann–Whitney at the beginning U test, of a with trial (Notean emphasis S3). The on initial consecutive two choices cor- rectof each responses trial were being critical made in at determining the beginning whether of a trial a parrot (Note wouldS3). The reach initial the two criterion. choices In of a eachnutshell, trial ρwere≥ 80% critical only in allows determining a parrot whet to makeher onea parrot incorrect would choice reach at the beginningcriterion. In of a a nutshell,trial. As thisρ ≥ 80% criterion onlymay allows be tooa parrot stringent to make (see resultsone incorrect below), choice we also at assessed the beginning the parrots’ of a trial.learning As this performance criterion may by considering be too stringen two othert (see adjustedresults below), learning we criteria, also assessed with ρ ≥ the0.75 par- (or rots’75%) learning and ρ ≥ performance0.7 (or 70%). by For considering each criterion, two we other counted adjust theed numberlearning of criteria, trials that with a birdρ ≥ 0.75took (or to 75%) reach and the learningρ ≥ 0.7 (or criterion 70%). For for each each criterion, pattern. Forwe eachcounted individual, the number the mean of trialsρ value that of each session was used to assess their learning performance with increased experience for each pattern. Exploration. To examine the macaws’ explorative behaviours, we recorded two be- haviours after each of them had completed the trial (as additional exploration after task completion may be useful to locate rewards): (1) the mean time (seconds) from when the Birds 2021, 2, FOR PEER REVIEW 7

a bird took to reach the learning criterion for each pattern. For each individual, the mean ρ value of each session was used to assess their learning performance with increased ex- perience for each pattern. Birds 2021, 2 291 Exploration. To examine the macaws’ explorative behaviours, we recorded two be- haviours after each of them had completed the trial (as additional exploration after task completion may be useful to locate rewards): (1) the mean time (seconds) from when the parrotparrot opened opened the the last last well well to to thethe timetime itit leftleft the box when they they experienced experienced a a change change on onthe the first first week week of of training training (i.e., the meanmean timetime ofof twotwo changes: changes: a a change change of of seeds seeds being being availableavailable in in all all wells wells during during the the habituation habituation phase, phase, to to nuts nuts being being available available in in half half of of the the wellswells during during the the main main training, training, and and a changea change from from food food locations locations in in pattern pattern A A to to food food locationslocations in in pattern pattern B), B), as as ‘exploration ‘exploration after after a change’;a change’; and and (2) (2) the the mean mean time time (in (in seconds) seconds) theythey spent spent on on the the table table after after completing completing the the task task across across all all trials. trials. LearningLearning strategy. strategy.To To examine examine the the macaws’ macaws’ learning learning strategy strategy in in this this task, task, we we used used the the searchsearch order order in in which which a parrota parrot opened opened the the wells, wells, to to reflect reflect on on their their movement movement (forward (forward or or sideways)sideways) (Figure (Figure4). As4). theAs the maximum maximum number number of correct of correct responses responses was 6 was in each 6 in trial, each our trial, focusour focus was on was the on order the order (and corresponding(and corresponding correct correct or incorrect or incorrect responses responses in each in pattern)each pat- oftern) these of initial these 6 initial choices. 6 choices. To obtain To the obtain mean th correcte mean responses correct responses made in themade first in six the choices, first six wechoices, divided we the divided total number the total of number correct responsesof correct maderesponses in the made first in 6 choicesthe first by 6 choices the total by numberthe total of number trials an of individual trials an individual participated part in.icipated We also in. obtained We also the obtained total number the total of number wells thatof awells parrot that opened a parrot for opened each trial for and each divided trial and this divided number this by its number time spent by its in time completing spent in thatcompleting trial (i.e., that the durationtrial (i.e., in the seconds duration between in seconds opening between the first opening well and the thefirst last well well), and to the obtainlast well), the mean to obtain time the taken mean to open time ataken well. to open a well.

FigureFigure 4. 4.Well Well numbers numbers assigned assigned on on the the poke poke box. box. A A parrot’s parrot’s movement movement on on the the poke poke box box can can be be → → categorisedcategorised into into two two types: types: moving moving forward forward (e.g., (e.g., 1 1→ 55 or or 6) 6) or or moving moving sideways sideways (e.g., (e.g., 11 11 →12).12). De- pending on the pattern (A or B), the search order also provides correct and incorrect responses as Depending on the pattern (A or B), the search order also provides correct and incorrect responses as well as the total number of wells opened for each trial. well as the total number of wells opened for each trial.

2.5.2.5. Data Data Analyses Analyses WeWe analysed analysed all all data data using using R R studio studio (version (version 1.1.463) 1.1.463) [37 [37]] and and SPSS SPSS (version (version 25) 25) (IBM (IBM Corp.).Corp.). As As differences differences in dietin diet composition composition have have been been shown shown to relate to relate to body to sizebody (and size thus (and weight)thus weight) in Neotropical in Neotropical parrots [parrots28], we [28], attempted we attempted to control to for control body weightfor body in weight all models, in all eithermodels, as an either additional as an additional random effect random in the effect GLMM in the model GLMM or as model a fixed or effect as a fixed in the effect GLM in modelsthe GLM (see models below). However,(see below). a Pearson’s However, r correlation,a Pearson’s that r correlation, was conducted that priorwas toconducted model fitting,prior to showed model afitting, close-to-perfect showed a close-to-perfect positive relationship positive between relationship species between (GG or species BT) and (GG weightor BT) (r and = 0.97). weight The (r attempted = 0.97). The inclusion attempted of weight inclusion also of resulted weight inalso convergence resulted in issues.conver- Accordingly,gence issues. our Accordingly, subsequent analysesour subsequent placed theanalyses focus onplaced our mainthe focus independent on our main variable, inde- species,pendent when variable, examining species, the parrots’when examining learning performance, the parrots’ theirlearning exploration performance, behaviour, their and learning strategy. The normality of the data was checked using the Shapiro–Wilk test when selecting the family and link distribution. To examine the parrots’ learning performance across sessions, we used a Generalised Linear Mixed Model with Binomial log link distribution to explore three main fixed effects, species (GG or BT), pattern (A or B) and session number (1–30), on the mean ρ value for each session across sessions of the unadjusted criterion (ρ ≥ 0.8). Individual identity was set as a random variable. Three Birds 2021, 2, FOR PEER REVIEW 8

exploration behaviour, and learning strategy. The normality of the data was checked us- ing the Shapiro–Wilk test when selecting the family and link distribution. To examine the parrots’ learning performance across sessions, we used a Generalised Linear Mixed Model Birds 2021, 2 with Binomial log link distribution to explore three main fixed effects, species (GG or BT),292 pattern (A or B) and session number (1–30), on the mean ρ value for each session across sessions of the unadjusted criterion (ρ ≥ 0.8). Individual identity was set as a random var- iable. Three Generalised Linear Models (GLM) with Poisson log link distribution were carriedGeneralised out to examine Linear Models the effect (GLM) of species with Poisson on the number log link distributionof trials taken were to reach carried each out of to theexamine learning the criteria effect ( ofρ ≥ species 0.8, ≥ 0.75, on the or ≥ number 0.7) for ofeach trials pattern taken (A to or reach B). To each examine of the species learning differencescriteria (ρ in≥ exploration0.8, ≥ 0.75, orbehaviour≥ 0.7) for and each learni patternng strategy, (A or B). another To examine five GLM species models differences with gaussianin exploration distributions behaviour were andused learning to examine strategy, the mean another time five (seconds) GLM modelsto open witha well, gaussian mean timedistributions to complete were a trial, used exploration to examine after the a mean change time (of (seconds) pattern), tomean open time a well, (seconds) mean timespent to oncomplete the table, a trial,and the exploration mean correct after aresponses change (of made pattern), in the mean first timesix choices. (seconds) A spenttwo-tailed on the significanttable, and test the was mean p ≤ correct 0.05. responses made in the first six choices. A two-tailed significant testFurther was p ≤ analyses0.05. on the parrots’ learning strategy in relation to a failure of learning a patternFurther (see below analyses for detail) on the were parrots’ conducted learning using strategy each inbird’s relation search to aorder. failure These of learning anal- ysesa pattern were mostly (see below descriptive for detail) and individual-b were conductedased. usingWe report each (1) bird’s the searchfrequency order. of using These ‘forward’analyses or were ‘sideways’ mostly search; descriptive (2) sideways and individual-based. responses that led We to report incorrect (1) the responses; frequency (3) of meanusing consecutive ‘forward’ or correct ‘sideways’ responses search; made (2) sideways on the responsesfirst six choices; that led and to incorrect (4) frequency responses; of (3) mean consecutive correct responses made on the first six choices; and (4) frequency of consecutive correct responses made in the first six choices. consecutive correct responses made in the first six choices.

3.3. Results Results 3.1.3.1. Learning Learning Performance Performance WithWith ρ ρ≥ ≥0.80.8,, none none ofof the the BT BT and and one one GG GG (Hagrid) (Hagrid) learned learned both both patterns. patterns. Learning Learning performanceperformance across across training sessionssessions diddid not not differ differ by by species species (GLMM: (GLMM: Z = −Z0.41, = −0.41,p = 0.680 p = ), 0.680),but did but differ did differ by pattern by pattern (Z = 15.27,(Z = 15.27,p < 0.001) p < 0.001) and trainingand training session session (Z = 3.69,(Z = 3.69,p < 0.001) p < 0.001)(Table (Table S1). Performance S1). Performance was betterwas better in pattern in pattern B than B pattern than pattern A (Figure A (Figure5), and 5), as trainingand as trainingprogressed. progressed. None None of the of macaws the macaws except ex onecept GG, one Hagrid,GG, Hagrid, learned learned pattern pattern A with A with both bothadjusted adjusted learning learning criteria criteria (ρ ≥(ρ 0.75≥ 0.75 and andρ ρ≥ ≥ 0.7).0.7). For pattern B, B, 4 4 BT BT and and all all GG GG reached reached ρ ρ≥ ≥0.75,0.75, and and all all macaws macaws reached reached ρ ρ≥ ≥0.70.7 (see (see supplementary Supplementary vi Videosdeos for for pattern pattern A Aand and patternpattern B). B). As As most most individuals individuals only only learned learned pattern pattern B, B, we we compared compared the the number number of of trials trials takentaken to to reach reach each each of of the the criteria criteria between between the the two two species. species. We We found found that that the the GG GG were were significantlysignificantly faster faster than than the the BT BT in in learning learning pattern pattern B Bregardless regardless of of whether whether the the criterion criterion 2 2 waswas adjusted adjusted (GLM: (GLM: ρ ρ≥ ≥0.8:0.8: χ21χ =1 60.21,= 60.21, p

Figure 5. Learning performance, indicated as mean ρ values of both species (N = 12), across training sessions for each pattern.

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Birds 2021, 2 293 Figure 5. Learning performance, indicated as mean ρ values of both species (N = 12), across training Figure 5. Learning performance, indicated as mean ρ values of both species (N = 12), across training sessions for each pattern. sessions for each pattern.

100 *** *** ** 80

60

40

20

0 BT GG BT GG BT GG criterion to reach Number of trials (N = 6) (N = 6) (N = 4) (N = 6) (N = 4) (N = 4)

ρ ≥ 0.7 ρ ≥ 0.75 ρ ≥ 0.8

FigureFigureFigure 6. 6. 6.Box BoxBox plot plot plot of of three of three three passing passing passing criteria, criteria, criteria, ρ ρ≥ ≥0.7ρ 0.7≥ (or 0.7(or 70%), (or70%), 70%), ρ ρ≥ ≥0.75 ρ0.75≥ (or 0.75(or 75%), 75%), (or and 75%), and ρ ρ≥ and ≥0.8 0.8 ρ(or ≥(or 80%),0.8 80%), (or to assess learning performance for pattern B for each species (BT = Blue-throated Macaws, GG = to 80%),assess to learning assess learningperformance performance for pattern for B pattern for each B forspecies each (BT species = Blue-throated (BT = Blue-throated Macaws, Macaws, GG = Great Green Macaws). *** p < 0.001, ** p < 0.01. GreatGG =Green Great Macaws). Green Macaws). *** p < 0.001, *** p <** 0.001,p < 0.01. ** p < 0.01.

3.2.3.2.3.2. Learning Learning Learning Strategy Strategy Strategy and and and Exploratory Exploratory Exploratory Behaviour Behaviour Behaviour AcrossAcrossAcross all all all trials trials (of (of both both patterns), patterns), the the BT BT took took significantly significantly significantly less less time time to to open open a a well well 22 thanthanthan the the GG GGGG (χ ((χ2χ1 1=1 ==9.77, 9.77,9.77, p p p== =0.002)0.002) 0.002) (Figure (Figure (Figure 77A,A, 7A, NoteNote Note S4, S4, S4, Table Table Table S3A) S3A) S3A) and and and to completeto to complete complete each each each trial 2 2 trialtrial(χ (1χ =(2χ1 10.60,=1 =10.60, 10.60,p = p 0.001,p= =0.001, 0.001, Median Median Median BT BT =BT 46.7= =46.7 46.7 s, GGs, s,GG =GG61.3 = =61.3 61.3 s, Figures, s,Figure Figure7B, 7B, Table 7B, Table Table S3B). S3B). S3B). When When When they theytheyfirst first experiencedfirst experienced experienced a change a achange change (of (of pattern) (of pattern) pattern) in thein in the first the first week,first week, week, the the mean the mean mean exploration exploration exploration time time aftertime 2 2 afteraftera change a achange change of pattern of of pattern pattern was was significantlywas significantly significantly less less in less the in in BTthe the than BT BT than inthan the in in GGthe the (χGG GG1 =(χ ( 4.35,2χ1 =1 =4.35, p4.35,= 0.037p p= =, 0.037,0.037,Table Table S3C)Table S3C) (Figure S3C) (Figure (Figure8A). On 8A). 8A). average, On On average, average, the mean th the timeemean mean spent time time onspent spent the tableon on the the was table table also was was significantly also also sig- sig- 2 2 nificantlynificantlyless in the less less BT in thanin the the inBT BT the than than GG in in ( χthe the1 =GG GG 7.72, (χ (2χ1p =1= =7.72, 0.005,7.72, p p= Table =0.005, 0.005, S3D) Table Table (Figure S3D) S3D)8 (FigureB). (Figure Compared 8B). 8B). Com- Com- with paredparedthe BT, with with the the GGthe BT, madeBT, the the significantlyGG GG made made significantly significantly more mean mo correct morere mean mean responses correct correct in responses theresponses first six in in responsesthe the first first six persix 2 2 χ 21 χ 21 responsesresponsestrial in pattern per per trial trial A (in in pattern1 pattern= 5.17, Ap A (=χ ( 0.023,2χ1 = =5.17, 5.17, Table p p= S3E)=0.023, 0.023, but Table Table not inS3E) S3E) pattern but but notB not ( in in1 pattern= pattern 0.95, pB =B(χ 0.329(2χ1 = =, 0.95,0.95,Table p p=S3F) =0.329, 0.329, (Figure Table Table9 S3F)). S3F) (Figure (Figure 9). 9).

FigureFigureFigure 7. 7.Box Box plot plot of of mean mean time time (s) (s) to to (A (A) open) open a awell well and andand (B (()B complete)) completecomplete a aatrial trialtrial (BT (BT(BT = ==Blue-throated Blue-throated Macaws,Macaws,Macaws, GG GG = Great= Great Great Green Green Green Macaws). Macaws). Macaws). ** ** **p

Birds 2021, 2 294 BirdsBirds 2021 2021, 2,, 2FOR, FOR PEER PEER REVIEW REVIEW 1010

FigureFigure 8.8. 8. BoxBox Box plots plots plots of of exploration-relatedof exploration-related exploration-related behaviours: behaviours: behaviours: (A) the( A(A) two)the the species’two two species’ species’ ‘exploration ‘exploration ‘exploration after a changeafter after a a changeofchange pattern of of pattern occurs, pattern measuredoccurs, occurs, measured measured as the mean as as the the duration mean mean du induration secondsration in in seconds from seconds opening from from opening theopening last wellthe the last tolast leavingwell well to to leavingtheleaving box the when the box box the when when parrots the the firstparrots parrots experience first first ex experience aperience change a inachange change the first in in week.the the first first (B week.) week. The mean(B ()B The) The time mean mean in seconds time time in in secondsspentseconds on spent the spent table on on the across the table table trials across across (BT trials =trials Blue-throated (BT (BT = =Bl Blue-throatedue-throated Macaws, Macaws, GGMacaws, = Great GG GG Green= =Great Great Macaws). Green Green Macaws). Macaws). * p < 0.05, * * p < 0.05, ** p < 0.01. **pp << 0.05, 0.01. ** p < 0.01.

Figure 9. Search order analysis on the mean of the first six correct responses per trial for pattern A FigureFigure 9. Search 9. Search order order analysis analysis on the on themean mean of the of thefirst first six correct six correct responses responses per pertrial trial for forpattern A (A) and pattern B (B). * p < 0.05. (A) patternand pattern A (A B) and(B). pattern* p < 0.05. B (B). * p < 0.05. 3.3. Search Order in Pattern A 3.3.3.3. Search Search Order Order in in Pattern Pattern A A Most macaws did not reach the criterion for pattern A, and so we analysed their MostMost macaws macaws did did not not reach reach the criterionthe criterion for pattern for pattern A, and A, so and we analysedso we analysed their search their search order to examine why they may have failed to do so. During a trial, the macaws ordersearch to examineorder to whyexamine they why may they have may failed have to do failed so. During to do so. a trial, During themacaws a trial, the frequently macaws frequently chose an adjacent well after making a choice (e.g., 1→2, 2→6 Figure 4). Their chosefrequently an adjacent chose well an adjacent after making well aafter choice making (e.g., 1a →choice2, 2 →(e.g.,6 Figure 1→2, 42).→ Their6 Figure movement 4). Their → movementtomovement an adjacent to to an wellan adjacent adjacent could bewell well categorised could could be be ca ascategorised twotegorised types: as as forwardtwo two types: types: (e.g., forward forward 2 → 6) (e.g., or(e.g., sideways 2 2→6)6) or or → sideways(e.g.,sideways 1 → 2)(e.g., (e.g., (Figure 1 1→2)42)). (Figure However,(Figure 4). 4). However, sideways However, movementssideways sideways movements movements would not facilitatewould would not not the facilitate macawsfacilitate the tothe macawsreachmacaws the to criterionto reach reach the the of criterion pattern criterion A.of of Wepattern pattern focused A. A. We onWe focused the focused unsuccessful on on the the unsuccessful unsuccessful individuals’ individuals’ individuals’ initial two initialchoicesinitial two two of eachchoices choices trial, of of whicheach each trial, trial, determined which which determined determined whether they whether whether would they they reach would wouldρ ≥ reach0.8 reach for ρ that ρ≥ ≥0.8 0.8 trial. for for thatIndeed,that trial. trial. all Indeed, Indeed, the BT all and all the the 4 GGBT BT and (except and 4 4GG GG Enya) (except (except mostly Enya) Enya) showed mostly mostly sideways showed showed sideways movement sideways movement movement (median: (median:BT:(median: 94.3%, BT: GG:BT: 94.3%, 94.3%, 95.6%) GG: GG: (Figure 95.6%) 95.6%) 10 (FigureA). (Figure Regardless 10A). 10A). Regardless Regardless of the outcome of of the the (correctoutcome outcome or (correct incorrect)(correct or or incor- of incor- the rect)firstrect) response,of of the the first first moving response, response, sideways moving moving to sideways ansideways (incorrect) to to an an adjacent(incorrect) (incorrect) well adjacent adjacent (e.g., 1 well →well2, (e.g., Figure(e.g., 1 →14→2,)2, wasFig- Fig- urepredominanture 4) 4) was was predominant predominant in all the BT in (median:in all all the the BT 87.1%)BT (medi (medi andan:an: one 87.1%) 87.1%) GG (Rita,and and one 100%)one GG GG (Figure(Rita, (Rita, 100%) 10100%)B). (Figure (Figure 10B).10B).

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Perhaps the unsuccessful macaws were using an alternative strategy, i.e., opening a well to indicate which pattern they should follow, or that they may have perceived pattern A as two separated columns (Figure 4). In both cases, the search order analysis in the first six responses of each trial should show that the parrots made three or more consecutive responses. We conducted an additional analysis of the first six responses (Note S5), which Birds 2021, 2 showed that the macaws did make consecutive correct responses (median proportion of295 trials with consecutive correct responses BT: 38.0%, GG: 17.8%, Figure 10C), however, they predominantly made 2 (instead of 3 or more) consecutive correct responses (Figure 10D).

B 1

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Figure 10. Search order in pattern A. A parrot may open another well by either going forward or sideways (see Figure4). The proportion of (A) sideways movement (from the first to the second choice), (B) sideways responses that lead to incorrect Figure 10. Search order in pattern A. A parrot may open another well by either going forward or sideways (see Figure 4). C D Theresponses; proportion ( ) of trials (A) withsideways consecutive movement correct (from responses the first made to the on second the first choice), six responses; (B) sideways and (responses) the consecutive that lead numberto incor- of rectcorrect responses; responses (C) trials made with in the consecutive first six choices correct (ranged responses from made 1–6, on coded the first in different six responses; colour). and (D) the consecutive num- ber of correct responses made in the first six choices (ranged from 1–6, coded in different colour). Perhaps the unsuccessful macaws were using an alternative strategy, i.e., opening a 4. wellDiscussion to indicate which pattern they should follow, or that they may have perceived pattern A as two separated columns (Figure4). In both cases, the search order analysis in the first sixThis responses study ofprovides each trial evidence should in show support that of the the parrots hypothesis made that three variation or more in consecutive diet and habitatresponses. specialisation We conducted affects an a species’ additional propen analysissity ofto thelearn first spatial six responses information (Note under S5), whichpre- dictableshowed spatial that theand macaws temporal did change. make consecutiveTwo closely correctrelated responsesmacaw species (median that proportionvary in diet of andtrials habitat with specialisation consecutive correct improved responses their BT:lear 38.0%,ning performance GG: 17.8%, Figureover the 10 C),course however, of train- they ing,predominantly despite the two made patterns 2 (instead varying of 3 or in more) their consecutivedifficulty. While correct both responses macaw(Figure species 10 ac-D). quired the easier pattern (pattern B), the relatively more generalist Great Green Macaws performed4. Discussion better overall than the more specialist Blue-throated Macaws. The Great Green This study provides evidence in support of the hypothesis that variation in diet and habitat specialisation affects a species’ propensity to learn spatial information under predictable spatial and temporal change. Two closely related macaw species that vary in diet and habitat specialisation improved their learning performance over the course of Birds 2021, 2 297

training, despite the two patterns varying in their difficulty. While both macaw species acquired the easier pattern (pattern B), the relatively more generalist Great Green Macaws performed better overall than the more specialist Blue-throated Macaws. The Great Green Macaws were faster in acquiring the spatial pattern B and reached a higher accuracy than the Blue-throated Macaws in pattern A. The fact that the more generalist Great Green Macaws showed better performance in acquiring spatial information than the more specialist Blue-throated Macaws, can be partially explained by the Great Green Macaws showing more exploration in general, and in particular, after a change occurs. Generalist species are predicted to be more explorative than specialists [10]. Concerning our tested species, however, we know little about their exploration behaviour. In a previous study on flexible and novel food-extraction problem solving, the two species did not differ in most exploration measures that were directly related to the problem (e.g., duration in touching the apparatus) [38]. However, exploratory behaviours allow individuals to obtain additional information in their environment [39], which could be seen in a more indirect way. In this study, our exploration measures were recorded after the individuals completed the task. The more generalist Great Green Macaws, on average, spent more time on the table and in particular, exploring more after a change of pattern occurred, than the Blue-throated Macaws. Increased exploratory behaviours in the Great Green Macaws may have helped them to take fewer trials to learn the easier pattern B and showed more correct responses for the more difficult pattern A, than the Blue-throated Macaws. Exploratory behaviours have been proposed as a pre- adaptive trait, along with behavioural flexibility, that can lead to successful establishment in new environments (e.g., [40]). A greater tendency to explore may thus relate to the wider diet spectrum and habitat range reported for Great Green Macaws compared to Blue-throated Macaws [22,24,25]. However, the relative role of exploration in relation to diet spectrum and habitat range, alongside other behavioural and personality traits such as neophobia [41,42], or tolerance in dealing with greater climate variation and environmental uncertainty associated with relatively larger brains [43], remains to be investigated. In addition to this, although exploratory behaviours have mostly been related to a species’ ecological background (e.g., diet and/or habitat specialisation) [10,39,44,45], exploratory behaviours have also been shown to vary within a species [46]. Such inter-individual variation in exploratory behaviour may relate to differences in how individuals seek and acquire information [46], which may relate to variations in making correct/incorrect choices or consecutive correct responses, as well as affecting individual specialisation in utilising different resources [47,48]. Another explanation for the species difference in performance may be related to the use of opposing speed vs. accuracy trade-off strategies, that in turn relate to the species’ diet and habitat specialisation. Compared with generalists, specialists tend to make faster decisions [9], and seem to pay more attention to environmental cues during foraging [5]. The Great Green Macaws on average spent more time opening wells and took longer to complete a trial than the Blue-throated Macaws, possibly reflecting that the Great Green Macaws traded-off speed for accuracy, whereas the Blue-throated Macaws traded-off accuracy for speed. Both strategies appear to be equally adaptive as it leads to the same outcome (collecting all rewards). The fast-but-inaccurate strategy that the Blue-throated Macaws employed may reflect their readiness in deploying certain specialised foraging skills (i.e., tearing the paper of the wells in this task), which in turn allows them to afford the costs of making errors. Similar to many humans [49] and non-human such as bumblebees (Bombus terrestris)[50,51], Indian Mynas (Sturnus tristis)[52], Carib Grackles (Quiscalus lugubris)[53], Ring-tailed Coatis (Nasua nasua)[54], and even in basal eukaryotic organisms like slime moulds (Physarum polycephalum)[55], the use of such strategies varies within species. While we observe individual variation in the use of these strategies within each species, the factors that affect an individual’s use of which learning strategy is not the main focus of this study and requires future investigations. Birds 2021, 2 298

In this study, we have adapted established paradigms that are used to examine spatial pattern learning (e.g., [13–16]). While paradigms used across studies vary depending on the examined research question (and thus, comparability of performance should be cautious), the ability to show spatial pattern learning has also been shown in bumblebees [56], Sprague-Dawley rats [13,14], Rufous Hummingbirds [16], to name a few. In this study, the macaws experienced two, arguably simple, recuring patterns in a predictable manner. However, only one Great Green Macaw learned both patterns. In general, the macaws showed a better learning performance for pattern B (wells located in the two middle columns) than pattern A (wells located at the two vertical edges of the poke box). This result seems counterintuitive in that pattern A should have provided visual cues, or direct internal (i.e., box edges) and external (e.g., wall colour) references for the macaws to locate the food. The use of visual cues is expected to enhance spatial pattern learning, as has been shown in, for example, human participants showing better performance when a visual cue is associated with either rewarded or non-rewarded locations [57]. While a previous study investigating spatial pattern learning in rats has also shown that visual cues facilitated rats to not revisit locations where they had retrieved rewards, visual cues did not necessarily enhance their spatial pattern learning [58]. The fact that the unsuccessful macaws showed a low proportion of correct responses and rarely made consecutive correct responses, indicates that they were neither using a strategy such as opening a well to infer the pattern as has been shown in rats [15] nor perceiving pattern A as two separated columns. Their poor performance in learning pattern A could be explained by the macaws mostly moving sideways. Such perseverance in moving sideways, in particular in the case of the Blue-throated Macaws, may reflect their restricted inhibitory control or inflexibility that has been reported in novel food-extraction problem-solving tasks [59]. However, we also consider the possibility that the macaws did not have to inhibit themselves, as their search strategies described above ultimately allow them to yield the maximum gain. Poorer performance in pattern A may also partly relate to the distance between rewarded choices: the two rewarded choices are adjacent to each other in pattern B but spread apart in pattern A. Accordingly, the parrots had a higher chance of making correct choices in pattern B by simply employing their “moving sideways” strategy. However, this led to a much lower success in pattern A.

5. Conclusions In summary, our study investigated the ability and speed of two closely related macaw species, with different ecological backgrounds, in acquiring spatial information in an eco- logically relevant foraging task. The more generalist Great Green Macaws outperformed the more specialist Blue-throated Macaws in learning performance over both spatial pat- terns, providing support for the hypothesis that generalist species learn spatial patterns faster, and thus, may adapt to change more easily. Such knowledge may provide rele- vant information for the conservation of these two critically endangered species, in that Blue-throated Macaws may be more vulnerable to changes in their natural environment.

Supplementary Materials: The following are available online at https://www.mdpi.com/article/ 10.3390/birds2030021/s1, Note S1: Housing, Note S2: Habituation (Pre-training phase), Note S3: Learning performance, Note S4: Search time analyses, Note S5: Search order analyses, Table S1: Result of a GLMM model with the effect of species (GG or BT), pattern (A or B), and training session on learning performance across training sessions, Table S2: Pattern B: Results of GLM models with a Poisson distribution that includes the effect of species (GG or BT) on the three learning criteria (ρ ≥ 0.8, ρ ≥ 0.75, and ρ ≥ 0.7), Table S3: Results of the GLM models with a Gaussian distribution that includes the effect of species (GG or BT) on the mean time (seconds) to open a well (A), to complete a trial (B), to explore after a change of pattern on the first week (C), spent on the table (D), as well as the mean correct responses made in the first six choices for pattern A (E) and pattern B (F), Video S1: Pattern A, Video S2: Pattern B. Author Contributions: P.K.Y.C. designed the experiment with input from J.R.D. and A.M.P.v.B.; P.K.Y.C. and J.R.D. conducted the experiment, wrote the protocol, ran the analyses, and wrote the Birds 2021, 2 299

first draft.; P.K.Y.C. and J.R.D. analysed all videos and A.B. conducted inter-rater reliability tests. All authors revised the manuscript and approved the submission. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by Mind Project to P.K.Y.C. Institutional Review Board Statement: Following the German Animal Welfare Act of 25 May 1998, Section 5, Article 7, and the Spanish Animal Welfare Act 32/2007 of 7 November 2007, Preliminary Title, Article 3, this study was classified as a non-animal experiment, and thus it did not require approval from a relevant body. The care and use of animals were strictly adhered to the ethical guidelines of the Association for the Study of Animal Behaviour and Animal Behaviour Society. Data Availability Statement: Data is available in OSF: DOI 10.17605/OSF.IO/FK62T. Acknowledgments: We thank Loro Parque, Wolfgang Kiessling, and his staff for their generous support and for providing us with access to the birds and the research facilities. We thank the Loro Parque Fundación and Christoph Kiessling, for their collaboration and the staff of the Loro Parque Fundación for their support. We are grateful to T. Boehly for assisting with the logistics for the experiment, M. Petelle for building parts of the apparatus, and A. Krasheninnikova for general advice and feedback on lab logistics. Conflicts of Interest: All authors declare there is no conflict of interest.

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