This study aimed to compare the extent of contrafreeloading in kea to that in Grey parrots, given that the two species exhibit very different levels of play: specifically, kea exhibit complex and frequent play29,30,35,36, whereas Greys exhibit considerably less play than several parrot species29. We found that, at the group level, although the overall amounts of kea classic contrafreeloading were nonsignificant, as a percentage of behaviour, kea generally contrafreeloaded more than Grey parrots in Experiment 1, whereas the opposite was true for Experiment 2. We compare the various behaviour patterns in detail, and propose explanations for our results below.
The most interesting comparisons for Smith et al.’s hypothesis are the results from classic contrafreeloading. In Experiment 1, kea performed this behaviour at non-negligible levels, given the supposed rarity of the behaviour5 (two birds at 50%; the others varying between 39 and 47%). In contrast, although one Grey did classically contrafreeload at a statistically significant level, the other three were at ≤ 36%. These data suggest that the kea may have found the task more engaging than did the Greys. However, given that only two kea chose to pop the lid of an empty cup in control trials significantly above chance, whereas three of the four Greys did so significantly above chance and one at chance, we doubt that the kea found the task inherently rewarding. We note that this comparison between both species must be interpreted cautiously due to differences in methodology: For the Greys, the control trials were performed at the end of the study, by which point they may have learnt to associate lid-popping with reward. However, the data from experimental trials in Smith et al.13 are such that their birds would have been primed in the opposite direction: For example, three of those four birds rarely chose the empty lidded cup when free food was available, nor did they classically or super contrafreeload to any significant extent13; an association-driven explanation is therefore unlikely. In contrast, the kea experienced this control condition at the start of the experiment, allowing them 20 trials to become acquainted with the affordances of both options that would be available throughout the study (lid-popping versus not lid-popping). This opportunity was important for kea, as this species has been previously shown to learn about object properties through extensive object manipulation37. That kea popped lids at or above chance in these first 20 control trials suggested two possibilities: (1) After these 20 trials, the task may have been familiar enough to no longer be of much interest (i.e., no longer novel and worthy of consideration) by the time rewarded trials began (recall nonsignificant downward trends for Harley Quinn and Blofeld). (2) They acquired some interest in popping the lids. This latter case seems more likely, as the lid-popping task still likely provided some added value. Kea engaged in non-negligible levels of classic contrafreeloading, such that the chance to pop a lid and eat could be considered more interesting than simply eating an identical but freely available reward. Furthermore, three kea chose a lidded, empty cup over a free, least-preferred reward at least half the time, again suggesting that the activity held some appeal of its own.
In Experiment 2 (which corresponds to classic contrafreeloading), all kea preferred freeloading for the walnut without a shell; two Greys, in contrast, nut contrafreeloaded at a statistically significant extent. This variability in behaviour at both the individual and species levels reveals the significance of a task’s proximate and potentially ultimate values in parrots’ choice to contrafreeload. Interestingly, although species like kea are hypothesized to prefer food items requiring high manipulation38,39, nut-cracking—chosen as an activity to provide direct comparison with the Greys13—is not prevalent in kea diet40, and that activity thus may not have been appropriate as an ethologically relevant one for kea. Greys, in contrast, are known to crack nuts in nature41. Future research could use a more ecologically relevant task for the kea, such as working to access food via digging or scraping32.
As with Smith et al.’s Greys13, kea in Experiment 1 performed calculated contrafreeloading to a statistically significant extent. All kea did so on over 83% of trials; for the Greys, three birds were close to 90% but one was at only 67%. Kea consistently selected their preferred food out of the two options provided, suggesting that the lid-popping action did not deter kea from selecting their preferred reward. In related trials, where the lid-status of food paired with an empty cup varied, kea, like some Greys13, preferred lidded food over an empty lidless cup, again showing that lid-popping for food was an acceptable task.
When examining situations in which food was discarded after contrafreeloading, we found that this choice in Experiment 1 was most common for Bruce. Notably, Bruce lacks a top mandible, making many of the manipulative behaviours more difficult to execute42. Bruce demonstrated consistent food preferences throughout the experiment, however, indicating that the reason some foods were discarded was, indeed, because they were too difficult for him to manipulate. In Experiment 2, Harley Quinn was the most likely to discard the nut, and did so exclusively in trials in which she chose the walnut without the shell (freeloaded). In these occasions, Harley Quinn was observed choosing the nut by tapping on it or the cup.
Like the Greys, the kea failed to super contrafreeload to a statistically significant extent. Furthermore, contrafreeloading trials in which a lid was popped but the food underneath was not consumed occurred most often with the least-preferred food. Given kea’s performance on control trials, the super contrafreeloading results are not surprising. Interestingly, when lid-status of food paired with an empty cup varied, some Greys very rarely—and depending on food desirability—preferred to pop the empty cup’s lid rather than consume the free food; as noted earlier, three of eight kea did so on at least half the trials when the food in the lidless cup was their least preferred option (sultanas). Both kea and Greys thus likely placed the appeal of the task along some “value scale” along with that of the available food rewards, the combination influencing their behaviour when the two variables were presented in various permutations. Notably, even in control trials, where no food was involved, no bird of either species found the task aversive, engaging in the behaviour at least 50% of the time. Future research could investigate how a different, more rewarding task would influence this balance and thus contrafreeloading for both species.
One possible alternative explanation for kea’s higher rates of contrafreeloading relative to those of Greys could be their natural tendency to probe and manipulate objects, thus causing them to pry off cup lids rather than manipulate lidless (open) cups. Were this action exploratory in nature, we would have observed significant decreases in behaviour as the experiment progressed, but note that we found no significant changes in any bird. Were they consistently drawn to lids and this behaviour were hard-wired, then we should have observed lid-popping appear significantly above chance across all three types of contrafreeloading. However, as discussed previously, kea did not significantly contrafreeload in the classic condition and actively freeloaded in super contrafreeloading conditions, suggesting that they were not simply interacting with lidded cups preferentially, but rather attending to the contents in the two cups and avoiding the additional manipulation of the lid when it led to a less (or, more often than not, equally) preferred food reward.
Another potential explanation for the differences observed between kea and Greys might be found in the theoretical overlap between contrafreeloading and play, and how individuals might view the contrafreeloading action as a type of play. As a seemingly nonfunctional, intrinsically motivating behaviour occurring in low-stress environments, incurring a positive mood, varying between conspecifics, and often incomplete and/or repeated14,15, play shares many proximate-level attributes with contrafreeloading13. Our results demonstrate that kea subjects inhabiting a low-stress, captive environment repeatedly chose to engage in classic contrafreeloading to a non-negligible extent and calculated contrafreeloading to a significant extent, varied in their behaviour between individuals, and at times, left the task incomplete (e.g., left food uneaten). Furthermore, evidence for intrinsic motivation to perform a given task is suggested by the kea’s overall differential behaviour between the two experiments, as well as inter-individual differences.
Importantly, this study serves only as a first step into determining whether play manifests as a form of contrafreeloading, but cannot ascertain that this is the only possible explanation for the presence or degree of contrafreeloading in the two species. Several alternative explanatory theories regarding the occurrence of contrafreeloading are enumerated in the discussion of Smith et al. (e.g., work ethic; information gathering; relief from boredom)13, and various other potential explanations (beyond playfulness) may reside at the species-level. Grey parrots (Psittacidae) and kea (Strigopidae) are separated by 50–80 million years of evolution43 and differ in their neurobiology (i.e., the size of the shell region related to vocal and possible cognitive abilities44). Differing ecological evolutionary pressures are also likely relevant: an island-based habitat39, a lack of natural predators30,45, and generalist diets40,46,47 are thought to have shaped the playfulness and cognitive abilities of kea30,40,46,47. Greys, in contrast, evolved predominantly on a continent (i.e., although they can be found on islands such as Principe, the Congo Grey is endemic to central Africa48,49), are subject to considerable predation48,50,51,52, and have a relatively less generalist diet (diverse but almost exclusively vegetarian and in which nuts play a significant role; see review in50). Such disparate evolutionary trajectories may offer other potential explanations for the differences in contrafreeloading observed between the two species, and future research could examine differences at genetic and/or neurological levels.
The varying rates of contrafreeloading observed between the species could have also been influenced by other factors. For example, although both parrot groups studied here inhabit enriched environments, are habituated to participating in experimental trials, and have access to food ad libitum, their habitats are markedly different. Notably, the Grey subjects live in “man-made” settings (i.e., Griffin and Athena in a lab; Pepper, Franco, and Lucci in private homes), whereas the kea inhabit a naturalistic zoo enclosure. Physical enrichment, although somewhat different in kind, is unlikely to have differed in quantity, as all birds are provided routine naturalistic foraging, and Lucci lives in a free-flight aviary. More likely is the difference in sociality: Relatively more subjects reside together in the kea group (15) compared to the Greys (two groups of two Greys and one Grey living with two birds of differing species), and thus variables such as social stimulation and flock-based foraging techniques could have contributed to the expression of contrafreeloading (note that subadult male kea are known to obtain food through kleptoparasitism32). In order to elucidate the role of habitat on contrafreeloading, future studies could examine the behaviour of species residing in more comparable captive conditions.
Future work should aim not only to apply these same methodologies to a broader range of parrot species, but also objectively quantify frequency and complexity of play across a wide range of parrots to allow a direct correlation between play and contrafreeloading over phylogeny in the parrot order. The apparent link between play behaviour and encephalisation in parrots53 offers another possible avenue for cross-species comparisons on contrafreeloading. Future research could also employ cognitive bias tests to quantify the mood of birds before and following contrafreeloading54, directly manipulate subjects’ participation in play behaviours or other control behaviours and observe whether engaging in play can increase contrafreeloading rates at the individual level, or perform behavioural coding of playfulness and/or arousal before and after contrafreeloading. Future research could incorporate more ecologically relevant contrafreeloading tasks to examine this behaviour at both the individual and species level, and approach the phenomenon by using both genetic and neuroscience techniques.
In sum, contrafreeloading is, by its very nature, an enigma whose study presents many difficulties. It varies across the diverse contexts within which it is studied, and given that it is rarely exhibited to a statistically significant extent, analyses that require comparing nonsignificant behaviour patterns across individuals and/or species is a challenging undertaking. Many explanations have been proposed, but contrafreeloading is still poorly understood, and its correlation with play is likely only one of several logical rationales. Nevertheless, our findings suggest that interest in play should not be discounted as a contributing factor.
Source: Ecology - nature.com
