Where’s the cookie? The ability of monkeys to track object transpositions

Where’s the cookie? The ability of monkeys to track object transpositions Object permanence is the ability to represent mentally an object and follow its position even when it has disappeared from view. According to Piaget’s 6-stage scale of the sensorimotor period of development, it seems that object permanence appears in Stage 4 and fully develops in Stage 6. In this study, we investigated the ability of some species of monkeys (i.e. pig-tailed macaque, lion-tailed macaque, Celebes crested macaque, barbary macaque, De Brazza’s monkey, L’Hoest’s monkey, Allen’s swamp monkey, black crested mangabeys, collared mangabeys, Geoffroy’s spider monkey) to track the displacement of an object, which consisted of a reward hidden under one of two cups. Our findings showed that the examined subjects possess Stage 6 of object permanence. We then compared our results with data on apes and dogs participating in Rooijakkers et al. (Anim Cogn 12:789–796, 2009) experiment, where the same method was applied. The monkeys examined by us performed significantly better than the dogs but worse than the apes. In our experiment, the monkeys performed above chance level in all variants, but it should be noted that we observed significant differences in the number of correct choices according to the level of a variant’s complexity. Keywords Object permanence · Transposition · Monkey · Ape · Dog · Piaget · Cognitive abilities Introduction perseveration error (Piaget 1954). Children between 12 and 18 months are able to find an object when it is hidden in Object permanence is defined as the ability to understand multiple locations within their view (Piagetian Stage 5), that objects continue to exist even when they have disap- but still have difficulties to find an object that is invisibly peared from view. In other words, if an object changes posi- displaced. The subject who reaches Stage 5 overcomes the tion, the subject is capable of mentally tracking the object’s perseveration error and takes into consideration succes- possible movements. This ability is considered to be the sive displacements. The full understanding of object per- fundamental skill of spatial cognition (Jaakkola 2014). manence develops in a human infant between the ages of According to Piaget’s 6-stage scale of sensorimotor devel- 18 and 24 months (Piagetian Stage 6). Then, a child can opment, it is only in Stage 4 that searching for a hidden solve sequential invisible displacements and reconstruct the object starts (8–12 months in human infants). However, if movements of an unperceived object (de Blois et al. 1998). these children see an object in its first location and then It is believed that reaching this stage marks a milestone in this is hidden in another place, then they will seek it in the children’s development (Piaget 1954). Object permanence former location. This response is named an A-not-B or a and the ability to track a displaced object seem to be very important for many animals because every day they have to remember the location of predators or resources such as * Katarzyna Majecka food. Piaget’s scale is also used to determine the degree of katarzyna.majecka@biol.uni.lodz.pl development of cognitive abilities in non-human species. So far, the solving of displacement tasks has come under Department of Experimental Zoology and Evolutionary Biology, Faculty of Biology and Environmental Protection, scrutiny [reviewed in Jaakkola (2014)] in such animals as University of Lodz, Banacha 12/16, 90-237 Łódź, Poland cats [reviewed in Shreve and Udell (2015)], dogs (Fiset and Department of Ecology and Vertebrate Zoology, Faculty LeBlanc 2007; Rooijakkers et  al. 2009), dolphins (Jaak- of Biology and Environmental Protection, University kola et al. 2010; Johnson et al. 2015), sea lions (Singer and of Lodz, Banacha 12/16, 90-237 Łódź, Poland Vol.:(0123456789) 1 3 604 Animal Cognition (2018) 21:603–611 Henderson 2015), dwarf goats (Nawroth et al. 2015), par- unintentional body language or gaze of the experimenter. rots (Pepperberg and Funk 1990), and corvids (Pollok et al. Associative learning might cause the animal to pass the 2000). Likewise, several species of monkey, such as long- test because they have learned simple associative rules tailed macaques (Schloegl et al. 2013), rhesus macaques such as ‘pick the location that the experimenter indicated’. (Filion et al. 1996) and cotton top tamarins (Neiworth et al. Although the Piagetian framework may have some limita- 2003), have become the subject of similar studies. Finally, tions, it is still very useful in examining and comparing great and lesser apes have also been examined (e.g. de Blois cognitive abilities of human and non-human animals (Pep- et al. 1998; Call 2003; Collier-Baker et al. 2006; Rooijakkers perberg 2002). et al. 2009; Anderson 2012). According to Amici et al. (2010), there is no overall Comparisons of the ability of object tracking have been clear-cut distinction in cognitive skills between apes and done in both non-human primates and children. Such com- monkeys, and existing differences have often been overes- parisons for infants and great apes have been carried out timated (Tomasello and Call 1997). However, due to mis- under varying degrees of difficulty (e.g. invisible and vis- cellaneous procedures applied in different experiments, it ible displacement). Findings have shown that children 19 is hard to make comparisons between species. For this rea- months, 2 years and 2.5 years old as well as great apes have son, we decided to apply the methods used by Rooijakkers very similar cognitive skills for dealing with the physical et al. (2009), who compared dogs and great apes in experi- world (Call 2001; Barth and Call 2006; Collier-Baker and ments on their ability to track visually object transposition. Suddendorf 2006; Herrmann et al. 2007). The purpose of this study was to investigate the ability According to Jaakkola’s (2014) classification, there are of some species of monkeys to track the displacement of three experimental methodologies to be applied for under- an object and to compare the results from the literature standing invisible displacement in non-human animals, on apes and dogs, to which the same method was applied namely, a Piagetian task, rotation and transposition. In a using the transposition task (Rooijakkers et al. 2009). In standard Piagetian task, the target object is hidden inside this study, we were also interested in evaluating how the the displacement device, which is subsequently placed under subjects solve problems depending on the level of a vari- one of three opaque containers. Next, the displacement ant’s complexity. device is removed and the experimenter shows the subject the empty device and then the subject starts to search for the object. In a rotation task, opaque containers are placed on a turntable. The experimenter places the target object under Methods one of the opaque containers and rotates the turntable (90° or 180°). The third type of task, transposition, requires that Ethical note the target object be placed directly in containers without the intermediate displacement device. Subsequently, one or The experiment was non-invasive, the subjects partici- two containers out of the two or three provided are moved. pated in it voluntarily and they were neither food nor water The way the cups are moved affects the level of difficulty of deprived for the testing. The study received the approval of the task. If the containers cross path or the empty container The Local Ethics Committee for Animal Experimentation moves into the initial position of the baited container, then (permit number 3/ŁB11/2016 of 18th January 2016) and it causes more difficulties for the subject to choose baited acted in accordance with the law from 15th January 2015 containers (Doré et al. 1996; Fiset and Plourde 2013; Jaak- on the protection of animals used for scientific purposes. kola 2014; Rooijakkers et al. 2009). In all three tasks (i.e. Piagetian, rotation, transposition), the subject possesses a mental representation of the situation and points by logical Subjects inference to the correct position of the target object invisibly moved (Jaakkola 2014). 19 monkeys (7 females and 12 males), born in captivity, To claim that a species understands invisible displace- participated in the experiment (Table  1). The monkeys ment, three factors must be controlled for or ruled out: were housed at zoos across Poland: in Łódź (six individu- sensory cues, social cues and associative learning. If these als), Warszawa (one individual), Wrocław (nine individu- factors are not controlled for, then they could affect the als) and Poznań (three individuals). All individuals lived results of experiments. Thanks to them, the animal could in indoor and outdoor enclosures, were fed their species- complete the task successfully without conceptual under- typical diet (vegetables, fruit, insects) and water was avail- standing of invisible displacement (Jaakkola 2014). Sen- able at all times. For all subjects, the experiment involved sory cues could be, e.g., smell in case of dogs or the abil- rewards hidden inside cups and transposition tasks were a ity to echolocate (cf. dolphins, bats). Social cues include new experience. 1 3 Animal Cognition (2018) 21:603–611 605 Table 1 Monkeys included in the experiment Subject (name) Species Sex Age (years) ZOO Cercopithecidae Old World Monkey  Grześ Pig-tailed macaque Macaca nemestrina (Linnaeus, 1766) Male 23 ZOO Łódź  Naomi Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Female 11 ZOO Łódź  Rani Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Female 21 ZOO Łódź  Woolfie Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Male 26 ZOO Łódź  Punio Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Male 13 ZOO Łódź  Taro Celebes crested macaque Macaca nigra (Desmarest, 1822) Male 17 ZOO Wrocław  Tyson Barbary macaque Macaca sylvanus (Linnaeus, 1758) Male 11 ZOO Wrocław  Lisbeth Barbary macaque Macaca sylvanus (Linnaeus, 1758) Female 2 ZOO Wrocław  Ries Barbary macaque Macaca sylvanus (Linnaeus, 1758) Male 11 ZOO Wrocław  Canail Barbary macaque Macaca sylvanus (Linnaeus, 1758) Male 9 ZOO Wrocław  Hiszpan De Brazza’s monkey Cercopithecus neglectus Schlegel, 1876 Male 16 ZOO Łódź  Holly L’Hoest’s monkey Cercopithecus lhoesti Sclater, 1899 Female 8 ZOO Wrocław  Pyza Allen’s swamp monkey Allenopithecus nigroviridis (Pocock, 1907) Female 19 ZOO Warszawa  Corso Black crested mangabey Lophocebus aterrimus (Oudemans, 1890) Male 19 ZOO Wrocław  Alf Collared mangabey Cercocebus torquatus (Kerr, 1792) Male 16 ZOO Wrocław  Olaf Collared mangabey Cercocebus torquatus (Kerr, 1792) Male 5 ZOO Wrocław Atelidae New World Monkey  Zosia Geoffroy’s spider monkey Ateles geoffroyi Kuhl, 1820 Female 18 ZOO Poznań Zuza Geoffroy’s spider monkey Ateles geoffroyi Kuhl, 1820 Female 18 ZOO Poznań  Colombo Geoffroy’s spider monkey Ateles geoffroyi Kuhl, 1820 Male 17 ZOO Poznań the reward after choosing the correct cup. In the situation Warm‑up when the subject pointed to the un-baited cup, E1 showed an empty cup and where the reward is, but subject did not The monkeys were tested in the indoor or outdoor enclosures get it. The warm-up phase was completed when the subjects in which they lived. Enclosure selection depended on factors touched one of the two cups (baited or un-baited) five times. such as good visibility of the platform by the subject, not At this stage, the experimenter did not manipulate the cups finding any trace of the subject’s anxiety, and weather condi- in the same way as during the actual part of the experiment. tions. A wooden platform (60 × 30 cm) was attached outside of a mesh panel. There were four small dots on the platform Procedure at a distance of 15 cm from each other indicating the loca- tion of the cups. Two identical opaque grey cardboard cups The experiment always started in the same way. The for- (diameter 8 cm, 9 cm high) were used in the experiment. ward-facing experimenter (E1), invariably the same per- During the experiment, fruit and insects (species-typical son, sat in front of the subject, separated by the mesh panel diet) were provided as a reward. and the platform, and obtained its attention by showing All subjects underwent a warm-up phase prior to the the reward. Once the subject focused on the task, E1 put experiment with the aim to familiarise them with the pro- the food reward on the platform (location 2 or 4; Fig. 1) cedure of disappearance of food under cups and receiving it and next showed two empty cups and then covered the after touching the cup. The warm-up phase took place at the reward with one of them. The initial position of the cups same location where the experiment was later carried out in all variants was always the same (location 2 and 4). using the same platform and cups. The platform was fixed to After hiding the reward, the experimenter instantly pro- the net and left for 1 h to give the subjects time to get used to ceeded to manipulate the cups. E1 simultaneously moved it. The warm-up phase was conducted by the experimenter the cups from initial to final positions in the following (E1). During this phase, the cups were randomly distributed way: the right-hand side cup with his right-hand and the over the whole surface of the platform, but never in the loca- left-hand side cup with his left hand. After the cups were tions where they were to be presented during the experiment. put in their final positions (Fig.  1), the subject could touch E1 showed the empty cups to the subject and then covered either of them. It was only when the subject had made the the reward with one of the cups. The individual received 1 3 606 Animal Cognition (2018) 21:603–611 session, none of the variants could be repeated more than twice in a row. The variants were implemented as follows: Variant 1 E1 grabbed the right cup with the right hand and the left cup with the left hand, then with one continu- ous movement he moved the cups so that the cup from location 2 would be placed on location 1, and the cup from location 4 on location 3. Variant 2 E1 grabbed the right cup with the right hand and the left cup with the left hand, then with one continu- ous movement he moved the cups so that the cup from location 2 would be found on location 1, and the cup from location 4 on location 2. Variant 3 E1 grabbed the right cup with the right hand and the left cup with the left hand. Then with one con- tinuous motion, so that the arms would cross over the platform, moved the cup from location 2 to location 3, and the cup from location 4 to location 1. Variant 4 E1 grabbed the right cup with the right hand and the left cup with the left hand. Then with one con- tinuous motion, so that the arms would cross over the platform, moved the cup from location 2 to location 3, and the cup from location 4 to location 2. Variant 5 E1 grabbed the right cup with the right hand and the left cup with the left hand. Then with one con- tinuous motion, so that the arms would cross over the platform, moved the cup from location 2 to location 4, and the cup from location 4 to location 2 (Fig. 1). After completion of the experiments, a control test was Fig. 1 Schematic representation of the five different transposition var - performed in which the experimenter (E1) covered the cups iants performed in this study (according to Rooijakkers et  al. 2009). while placing the food to prevent the subject from knowing The grey cups represent the initial position, while the white ones indi- where it was hidden. The control procedure resembled the cate the final position in given variants if the cups were relocated. In experiment, but the monkey received the reward regardless all variants the start locations were the same. The order of the vari- ants presented by E1’s point of view: 2R, 5L, 1L, 3R, 4L, 5R, 1R, of the cup choice. The control test aimed at the exclusion of 3L, 4R, 2L, 2R, 5R, 1L, 3R, 4L, 5L, 1R, 3L, 4R, 2L (L, reward under such factors as the use of scent or unconscious hints given left–hand cup; R, reward under right-hand cup) by E1. The subjects entered the experiment voluntarily and could stop the experiment at any moment, departing from the place where it was carried out. Some subjects completed right choice that it received the hidden reward. The second the experiment during one session, whereas some subjects experimenter (E2), facing downwards, was present during lost interest in working with the experimenter. The experi- all trials, read out the subsequent numbers of the vari- ment was continued when the subject again approached the ants and noted whether the selection made by the subject place of the experiment. was correct or not. All the subjects underwent the experi- ment in the presence of five variants, each of them applied Data scoring and analysis four times, summing up to 20 trials total. Determined by drawing lots at the outset of the experiment, the order of Differences between variants were analysed by the ANOVA performing the random sequence of variants remained the Friedman test. In case of significant effects, a post hoc test same for each subject. The conditions of drawing lots stip- (Conover-Iman) was conducted. Second, the Wilcoxon test ulated that in each of the five task variants the food should was used to determine whether the results of the experiment be hidden twice under the right-hand side cup and twice in each variant were above chance. Third, differences (calcu- under the left-hand side one. What is more, during one lated separately for each variant) were investigated between 1 3 Animal Cognition (2018) 21:603–611 607 the results of the experiment and the control test using a non- Table 3 Results of post hoc Conover-Iman test comparing results of examined monkeys depends on variant of experiment (P value) parametric exact two-tailed statistic (Wilcoxon test). Finally, the findings obtained from the studied monkeys were com- Variant 1 Variant 2 Variant 3 Variant 4 Variant 5 pared with the raw scores of dogs and apes as available from Variant 1 the literature (Rooijakkers et al. 2009). To determine dif- Variant 2 0.285 ferences between dogs (N = 20) and monkeys (N = 19), and Variant 3 0.021 0.205 between apes (N = 8) and monkeys, the Mann–Whitney U Variant 4 0.002 0.030 0.349 test was performed separately for each variant. Variant 5 0.003 0.055 0.503 0.789 Significant values are highlighted in bold Results The individual results of the subjects tested in each variant examined monkeys performed above chance in all variants are shown in Table 2. (Wilcoxon test z > 2.65, P < 0.01 in all variants) (Fig. 2). When treated as a group, the subjects showed significant Differences between variants differences between the performance of the experiment to the result of the control test in each variant, which A significant effect of variant was observed (ANOVA excludes other external factors affecting selection of the Friedman test χ = 13.40, n = 19, df = 4, P < 0.01). Post cup during the test (Table 4). hoc Conover-Iman test showed that monkeys performed better in Variant 1, where both cups were moved to new locations without crossing each other’s path, compared Comparison of results with dogs and apes to Variants 3, 4 and 5, where cups crossed each other’s path. The subjects also achieved better results in Variant The monkeys subjected to the experiment achieved signifi- 2, where one cup moved to a new location and then substi- cantly better results than dogs (as reported in Rooijakkers tuted the initial location of the first without crossing each et al. 2009) in all five variants (Z > − 4.83, P ≤ 0.001 in all other’s path, compared to Variant 4 (Table 3). Overall, the cases Table 5; Fig. 2). However, the monkeys scored worse than apes (Rooijakkers et al. 2009) in Variant 2, 3, 4 and Table 2 Sum of correct choices Subjects Species Variant of each subject per variant (with four trials in each variant) 1 2 3 4 5 Grześ Pig-tailed macaque 3 3 3 2 4 Naomi Lion-tailed macaque 4 4 4 4 4 Rani Lion-tailed macaque 4 3 2 2 3 Woolfie Lion-tailed macaque 3 3 3 4 3 Punio Lion-tailed macaque 4 3 3 2 1 Taro Celebes crested macaque 3 3 3 3 4 Tyson Barbary macaque 3 4 3 4 3 Canail Barbary macaque 4 4 4 4 3 Ries Barbary macaque 4 3 4 4 4 Lisbeth Barbary macaque 4 3 2 2 3 Hiszpan De Brazza’s monkey 4 4 4 1 3 Holly L’Hoest’s monkey 4 4 4 2 2 Pyza Allen’s swamp monkey 4 3 2 2 2 Corso Black crested mangabey 4 3 4 4 3 Alf Collared mangabey 4 4 4 4 3 Olaf Collared mangabey 4 4 3 4 4 Zosia Geoffroy’s spider monkey 4 4 3 2 2 Zuza Geoffroy’s spider monkey 4 4 3 2 3 Colombo Geoffroy’s spider monkey 3 3 3 2 3 1 3 608 Animal Cognition (2018) 21:603–611 a, b a, b a, b Fig. 2 Mean number (± SEM) a a, b of correct response of the monkeys (N = 19) in the current study and the dogs (N = 20) and monkeys the apes (N = 8) from Rooijak- apes* kers et al. (2009) for each of the five variants. Statistically dogs* significant differences between the dogs and the monkeys (P < 0.01). statistically sig- nificant differences between the monkeys and the apes (P < 0.05) CHANCE Variant 1Variant 2Variant 3Variant 4Variant 5 * -Rooijakkerset al. (2009) Table 4 Wilcoxon test results subjects to track the position and find the hidden reward T z P comparing the performance of if the cups did not cross each other’s path during move- the subjects to the result of the Variant 1 0 3.62 < 0.001 ments. In fact, the monkeys obtained worse results if the control test Variant 2 0 3.62 < 0.001 paths of the two cups were crossed and the two containers Variant 3 9 3.05 0.01 exchanged locations with one another. Although monkeys Variant 4 5 2.67 0.01 performed above chance level in all variants, they scored Variant 5 15 2.13 0.03 significantly worse than the apes examined by Rooijakkers et al. (2009), except for Variant 1. In the latter experiment, which employed exactly the same procedure of this study, chimpanzees, bonobos, orangutans and gorillas succeeded 5. It was only in Variant 1 that no statistically significant differences were noted (Table  5; Fig. 2). in all variants, and the level of difficulty did not affect the results of the apes (Rooijakkers et al. 2009). In another experiment using a Piagetian task, which involved object transposition in the presence of the above-mentioned ape Discussion species, all subjects selected the correct cup above chance level and there were no significant differences amongst In the present study using the transposition task, monkeys were successful in all variants, both in the case of a sim- single and double (the reward changed the position twice) displacement tasks (Barth and Call 2006). Call (2001) ple displacement of the two cups and in displacements with reverse swapping. However, there were differences observed that orangutans, chimpanzees and 26-month- old children performed above chance level on visible in the number of correct choices according to the level of a variant’s complexity. Generally, it was easier for the and invisible displacement tasks, except for nonadjacent Table 5 Comparison of Comparison Monkeys Apes Dogs Monkeys/dogs Monkeys/apes the results of the examined monkeys and dogs and the Mean (± SD) Mean (± SD) Mean (± SD) Z P Z P results of monkeys and apes Variant 1 3.74 (± 0.45) 4.00 (± 0.00) 2.85 (± 0.88) − 3.23 0.001 1.54 0.12 [data on dogs and apes from Rooijakkers et al. (2009)] Variant 2 3.47 (± 0.51) 4.00 (± 0.00) 2.30 (± 1.08) − 3.57 < 0.001 2.51 0.01 (Mann–Whitney U test) Variant 3 3.21 (± 0.71) 3.88 (± 0.35) 1.85 (± 0.59) − 4.59 < 0.001 2.33 0.02 Variant 4 2.84 (± 1.07) 3.75 (± 0.46) 1.65 (± 0.81) − 3.21 0.001 2.02 0.04 Variant 5 3.00 (± 0.82) 3.63 (± 1.06) 1.00 (± 0.92) − 4.83 < 0.001 2.26 0.02 1 3 Animal Cognition (2018) 21:603–611 609 invisible displacements (i.e. the reward was moved to a social world. In nature, apes are forced to gain food from nonadjacent container). In another of Call’s (2003) experi- hidden locations (e.g. underground nests), which requires ments, several tasks were presented to chimpanzees and causal understanding, and sometimes they need to use a tool. orangutans. In the no-landmark transposition (food is pre- Probably because of this, they have evolved to develop skills sented directly to the subject), apes performed better than in reading causal cues (Bräuer et al. 2006). in the landmark (the subject had to infer the position of Dogs are considered to have an ability to read human the reward using a landmark) transposition test, whereas behaviour and use triadic communication, i.e. one individ- in the latter subjects obtained significantly better results in ual informs another about the location of various things, the no-swap transposition compared to the reverse swap. including food resources, for example, by pointing or other Overall, the results obtained by monkeys vary among gestures. Their skills in understanding cooperative signs experiments using a Piagetian task. For instance, long- have developed over thousands of years of domestication tailed macaques performed above chance level in single (Coppinger and Coppinger 2002; Hare and Tomasello 2005; and double transpositions (Amici et al. 2010), spider mon- Bräuer et al. 2006). On the other hand, as a result of domesti- keys only in a single transposition, but neither coped with cation, dogs could have lost some skills necessary for causal a reverse transposition, that is, when the baited cup and understanding due to lack of subsistence problems thanks to empty cup switched location twice and returned to their humans (Bräuer et al. 2006; Rooijakkers et al. 2009; Wynne original position. Experiments on cotton top tamarins 2016). Furthermore, ontogenetic development of interspe- revealed that their performance was above chance level cies cooperative skills in a dog may well result from the in both visible and invisible displacement tasks and only relationship established with a human in the first weeks of in one (i.e. double invisible displacement with the second its life, which is usually not the case with primates subjected cup manipulated by the experimenter) did results dropped to experiments (Miklósi et al. 2003; Wynne et al. 2008). to chance level (Neiworth et al. 2003). Even though the According to the hypothesis of Natale et al. (1986), mon- procedures adopted in the aforementioned experiments keys’ progress is limited to Stage 5 on the Piagetian scale differed, it is certain that a transposition which comprises of sensorimotor development of object permanence. The crossing paths poses difficulty to many species of pri- authors of that study presumed that only apes, hence not mates. It is solely apes that tackled such tasks successfully monkeys, could solve a task with the use of mental repre- regardless of difficulty level. sentation. However, the results of the present experiments as The monkeys used in the present experiment scored well as those of other researchers have given evidence for the significantly better in all tasks than the dogs examined by reaching of Stage 6 by the examined monkeys. The species Rooijakkers et al. (2009), which performed above chance of monkeys that demonstrated good cognitive abilities is the only in Condition 1 (i.e. both containers moved to a new cotton top tamarin, and results have shown that they possess location and not crossing each other’s path). If the containers Stage 6 object permanence (Neiworth et al. 2003). On the changed their position in such a way that they crossed each other hand, another monkey species, namely, the squirrel other’s path, then the dogs could not follow the transition monkey, did not possess this stage (de Blois et al. 1998). of the reward. This seems to indicate that monkeys exhibit Amongst primates, it was only lemurs that demonstrated more flexibility in mental representation compared to dogs. Stage 5 of object permanence, as they failed in invisible dis- Rooijakkers et al. (2009) assumed that great apes use their placement tasks—a result explained by Deppe et al. (2009) mental representation more flexibly than dogs. Undoubt- to be of ecological relevance. According to their hypothesis, edly, one must also concur with Rooijakkers et al. (2009), lemurs’ ability to obtain stationary fruit or leaves and to who noted that dog inferential abilities are better expressed avoid predators such as raptors, snakes and viverrids does in the olfactory than in the visual modality. Moreover, dif- not have to go beyond solving a visible displacement task. ferences in cognitive abilities between dogs and primates Lemurs are attacked by fossas, a large cat-like carnivore in are well illustrated by Bräuer et al.’s (2006) research. Their Madagascar, only during sleep. Snakes hunt them using sit- experiments showed that dogs perform better at finding hid- and-wait tactics, whereas raptors observed through foliage den food using communicative cues given by the human can appear in and disappear from the field of view (Good- experimenter, whereas apes do better when the reward man 2003). On the other hand, in animals which are at risk causes a noticeable change in the physical world (e.g. by of attack by terrestrial stalking predators such as felines, generating a noise). Generally, the cup manipulated by the possessing Stage 6 object permanence is very important experimenter was preferred by the examined dogs and they (Deppe et al. 2009). achieved almost 50% better results than the apes in under- In the case of non-primate animals, some species standing communicative cues (Bräuer et al. 2006). The latter of birds can achieve a high level of cognitive abilities. experiment provided arguments for apes’ developed ability Four species of parrots (i.e. an African Grey parrot, an to make inferences about the working of the physical and Illiger macaw, a cockatiel, and a parakeet) showed Stage 1 3 610 Animal Cognition (2018) 21:603–611 credit to the original author(s) and the source, provide a link to the 6 competence (Pepperberg and Funk 1990), and this level Creative Commons license, and indicate if changes were made. was also achieved by Eurasian jays (Zucca et al. 2007). Zucca et al. (2007) concluded that a Stage 5 competence would suffice for those birds to collect food, even though it is not enough for protecting their caches of food. Suc- References cessful protection of food is probably associated with the understanding of intentions and the manipulation of poten- Amici F, Aureli F, Call J (2010) Monkeys and apes: are their tial pilferers (Clayton and Dickinson 1998). cognitive skills really so different? Am J Phys Anthropol The human brain was designed by natural selection to 143:188–197 Anderson MR (2012) Comprehension of object permanence and sin- solve adaptive problems faced by our hunter–gatherer ances- gle transposition in gibbons. Behaviour 149:441–459. https :// tors (Duchaine et al. 2001). Obviously, the same process can doi.org/10.1163/15685 3912X 63976 9 be observed by examining the brain and adaptations in non- Barth J, Call J (2006) Tracking the displacement of objects: a series human species. The importance of cross-species compari- of tasks with great apes (Pan troglodytes, Pan paniscus. Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapi- sons to test evolutionary functions of organismic design is ens). J Exp Psychol Anim Behav Process 32(3):239–252 highly emphasised by evolutionary biologists, comparative Bräuer J, Kaminski J, Riedel J, Call J, Tomasello M (2006) Making psychologists, and behavioural ecologists. In this respect, inferences about the location of hidden food: social dog, causal an analysis of results regarding cognitive traits showed that ape. J Comp Psychol 120(1):38–47 Call J (2001) Object Permanence in Orangutans (Pongo pygmaeus), they probably evolved independently amongst several ver- Chimpanzees (Pan troglodytes), and Children (Homo sapiens). tebrate groups including Primates (Reader et al. 2011; van J Comp Psychol 115(2):159–171 Horik et al. 2012). The results of the examined species of Call J (2003) Spatial rotations and transpositions in orangutans monkeys, as well as data from the literature on corvids, par- (Pongo pygmaeus) and chimpanzees (Pan troglodytes). Primates 44:347–357 rots, cetaceans, and apes, showed that the understanding of Clayton NS, Dickinson A (1998) Episodic-like memory during cache object permanence in such species is at a similar stage of recovery by scrub jays. Nature 395:272–278 development (Stage 6 competence). According to van Horik Collier-Baker E, Suddendorf T (2006) Do Chimpanzees (Pan trog- et al.’s (2012) hypothesis, cognitive traits might have arisen lodytes) and 2-year-old children (Homo sapiens) understand double invisible displacement? J Comp Psychol 120(2):89–97 in distantly related groups (e.g. corvids and apes) because Collier-Baker E, Davis JM, Nielsen M, Suddendorf T (2006) Do they have evolved to solve similar environmental problems. chimpanzees (Pan troglodytes) understand single invisible dis- Having analysed many biological, ecological, behavioural placement? Anim Cogn 9:55–61 and social system traits, the authors of that study conclude Coppinger R, Coppinger L (2002) Dogs: a new understanding of canine origin, behaviour and evolution. Chicago University that, despite having different brain structures, there are strik - Press, Chicago ing similarities in the diet, use of tools, and social systems in de Blois ST, Novak MA, Bond M (1998) Object permanence in corvids, parrots, apes, cetaceans, and elephants. Van Horik Orangutans (Pongo pygmaeus) and Squirrel Monkeys (Saimiri et al.’s (2012) study also speculated that species character- sciureus). J Comp Psychol 112(2):137–152 Deppe AM, Patricia C, Wright PC, Szelistowski WA (2009) Object ised by a relatively large brain and that undergo a long devel- permanence in lemurs. Anim Cogn 12:381–388 opmental period, that live a long life and live in a fluctuating Doré FY, Fiset S, Goulet S, Dumas MC, Gagnon S (1996) Search habitat, could all be considered candidates for convergent behavior in cats and dogs: interspecific differences in working evolution of cognitive abilities. It is, therefore, believed that memory and spatial cognition. Anim Learn Behav 24:142–149. https ://doi.org/10.3758/BF031 98962 the monkeys studied in the present experiment match well Duchaine B, Cosmides L, Tooby J (2001) Evolutionary psychology with the aforementioned groups of vertebrates. Finally, it is and the brain. Curr Opin Neurobiol 11:225–230 worthwhile to investigate further the cognitive abilities of Filion CM, Washburn DA, Gulledge JP (1996) Can monkeys other, hitherto not yet examined species, and particularly (Macaca mulatta) represent invisible displacement? J Comp Psychol 110(4):386–395 monkeys, because some major advances in our understand- Fiset S, LeBlanc V (2007) Invisible displacement understanding ing of evolution have resulted from a convergence of data in domestic dogs (Canis familiaris): the role of visual cues in from numerous species (Sell 2012). search behaviour. Anim Cogn 10:211–224 Fiset S, Plourde V (2013) Object permanence in domestic dogs Acknowledgements We sincerely thank the Lodz ZOO, the Warsaw (Canis lupus familiaris) and gray wolves (Canis lupus). J Comp ZOO, the Poznan ZOO and the Wroclaw ZOO for allowing us to con- Psychol 127:115–127. https ://doi.org/10.1037/a0030 595 duct the experiments. We wish to thank the staff for their cooperation Goodman SM (2003) Predation on lemurs. In: Goodman SM, Ben- and patience during this project. stead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1221–1228 Hare B, Tomasello M (2005) Human-like social skills in dogs? Open Access This article is distributed under the terms of the Crea- Trends Cogn Sci 9:439–444 tive Commons Attribution 4.0 International License (http://creat iveco Herrmann E, Call J, Hernández-Lloreda MV, Hare B, Tomasello mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- M (2007) Humans have evolved specialized skills of social tion, and reproduction in any medium, provided you give appropriate 1 3 Animal Cognition (2018) 21:603–611 611 cognition: the cultural intelligence hypothesis. Science Piaget J (1954) The construction of reality in the child. Basic Books, 317:1360–1366 New York Horik JO, Clayton NS, Emery NJ (2012) Convergent evolution of Pollok B, Prior H, Güntürkün O (2000) Development of object per- cognition in corvids, apes and other animals. In Shackelford TK, manence in food-storing magpies (Pica pica). J Comp Psychol Vonk J (eds), The Oxford handbook of comparative evolution- 114(2):148–157 ary psychology. The Oxford University Press, Oxford Reader SM, Hager Y, Laland KN (2011) The evolution of pri- Jaakkola K (2014) Do animals understand invisible displacement? A mate general and cultural intelligence. Philos Trans R Soc B critical review. J Comp Psychol 128(3):225–239 366:1017–1027 Jaakkola K, Guarino E, Rodriguez M, Erb L, Trone M (2010) What Rooijakkers EF, Kaminski J, Call J (2009) Comparing dogs and great do dolphins (Tursiops truncatus) understand about hidden apes in their ability to visually track object transpositions. Anim objects? Anim Cogn 13:103–120 Cogn 12:789–796 Johnson CM, Sullivan J, Buck CL, Trexel J, Scarpuzzi M (2015) Vis- Schloegl C, Waldmann MR, Fischer J (2013) Understanding of and rea- ible and invisible displacement with dynamic visual occlusion soning about object–object relationships in long-tailed macaques? in bottlenose dolphins (Tursiops spp). Anim Cogn 18:179–193 Anim Cogn 16:493–507 Miklósi A, Kubinyi E, Topál J, Gácsi M, Virányi Z, Csányi V (2003) Sell AN (2012) Evolved cognitive adaptations. In: Shackelford TK, A simple reason for a big difference: wolves do not look back at Vonk J (eds) The Oxford handbook of comparative evolutionary humans, but dogs do. Curr Biol 13:763–766 psychology. The Oxford University Press, Oxford Natale F, Antinucci F, Spinozzi G, Poti P (1986) Stage 6 object concept Shreve KRV, Udel MAR (2015) What’s inside your cat’s head? A in nonhuman primate cognition: a comparison between Gorilla review of cat (Felis silvestris catus) cognition research past, pre- (Gorilla gorilla gorilla) and Japanese Macaque (Macaca fuscata). sent and future. Anim Cogn 18:1195–1206 J Comp Psychol 100(4):335–339 Singer R, Henderson E (2015) Object permanence in marine mam- Nawroth C, von Borell E, Langbein J (2015) Object permanence in the mals using the violation of expectation procedure. Behav Proc dwarf goat (Capra aegagrus hircus): perseveration errors and the 112:108–113 tracking of complex movements of hidden objects. Appl Anim Tomasello M, Call J (1997) Primate cognition. Oxford University Behav Sci 167:20–26 Press, New York Neiworth JJ, Steinmark E, Basile BM, Wonders R, Steely F, DeHart C Wynne CDL (2016) What is special about dog cognition? Curr Dir (2003) A test of object permanence in a new-world monkey spe- Psychol Sci 25(5):345–351 cies, cotton top tamarins (Saguinus oedipus). Anim Cogn 6:27–37 Wynne CDL, Udell MAR, Lord KA (2008) Ontogeny’s impacts on Pepperberg IM (2002) The value of the Piagetian framework for com- human-dog communication. Anim Behav 76:e1–e4. https ://doi. parative cognitive studies. Anim Cogn 5:177–182org/10.1016/j.anbeh av.2008.03.010 Pepperberg IM, Funk MS (1990) Object permanence in four species Zucca P, Milos N, Vallortigara G (2007) Piagetian object permanence of psittacine birds: an African Grey parrot (Psittacus erithacus), and its development in Eurasian jays (Garrulus glandarius). Anim an Illiger mini macaw (Ara maracana), a parakeet (Melopsittacus Cogn 10:243–258 undulatus), and a cockatiel (Nymphicus hollandicus). Anim Learn Behav 18(1):97–108 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Animal Cognition Springer Journals

Where’s the cookie? The ability of monkeys to track object transpositions

Free
9 pages
Loading next page...
 
/lp/springer_journal/where-s-the-cookie-the-ability-of-monkeys-to-track-object-2VZv9oaDNN
Publisher
Springer Berlin Heidelberg
Copyright
Copyright © 2018 by The Author(s)
Subject
Life Sciences; Behavioral Sciences; Zoology; Psychology Research
ISSN
1435-9448
eISSN
1435-9456
D.O.I.
10.1007/s10071-018-1195-x
Publisher site
See Article on Publisher Site

Abstract

Object permanence is the ability to represent mentally an object and follow its position even when it has disappeared from view. According to Piaget’s 6-stage scale of the sensorimotor period of development, it seems that object permanence appears in Stage 4 and fully develops in Stage 6. In this study, we investigated the ability of some species of monkeys (i.e. pig-tailed macaque, lion-tailed macaque, Celebes crested macaque, barbary macaque, De Brazza’s monkey, L’Hoest’s monkey, Allen’s swamp monkey, black crested mangabeys, collared mangabeys, Geoffroy’s spider monkey) to track the displacement of an object, which consisted of a reward hidden under one of two cups. Our findings showed that the examined subjects possess Stage 6 of object permanence. We then compared our results with data on apes and dogs participating in Rooijakkers et al. (Anim Cogn 12:789–796, 2009) experiment, where the same method was applied. The monkeys examined by us performed significantly better than the dogs but worse than the apes. In our experiment, the monkeys performed above chance level in all variants, but it should be noted that we observed significant differences in the number of correct choices according to the level of a variant’s complexity. Keywords Object permanence · Transposition · Monkey · Ape · Dog · Piaget · Cognitive abilities Introduction perseveration error (Piaget 1954). Children between 12 and 18 months are able to find an object when it is hidden in Object permanence is defined as the ability to understand multiple locations within their view (Piagetian Stage 5), that objects continue to exist even when they have disap- but still have difficulties to find an object that is invisibly peared from view. In other words, if an object changes posi- displaced. The subject who reaches Stage 5 overcomes the tion, the subject is capable of mentally tracking the object’s perseveration error and takes into consideration succes- possible movements. This ability is considered to be the sive displacements. The full understanding of object per- fundamental skill of spatial cognition (Jaakkola 2014). manence develops in a human infant between the ages of According to Piaget’s 6-stage scale of sensorimotor devel- 18 and 24 months (Piagetian Stage 6). Then, a child can opment, it is only in Stage 4 that searching for a hidden solve sequential invisible displacements and reconstruct the object starts (8–12 months in human infants). However, if movements of an unperceived object (de Blois et al. 1998). these children see an object in its first location and then It is believed that reaching this stage marks a milestone in this is hidden in another place, then they will seek it in the children’s development (Piaget 1954). Object permanence former location. This response is named an A-not-B or a and the ability to track a displaced object seem to be very important for many animals because every day they have to remember the location of predators or resources such as * Katarzyna Majecka food. Piaget’s scale is also used to determine the degree of katarzyna.majecka@biol.uni.lodz.pl development of cognitive abilities in non-human species. So far, the solving of displacement tasks has come under Department of Experimental Zoology and Evolutionary Biology, Faculty of Biology and Environmental Protection, scrutiny [reviewed in Jaakkola (2014)] in such animals as University of Lodz, Banacha 12/16, 90-237 Łódź, Poland cats [reviewed in Shreve and Udell (2015)], dogs (Fiset and Department of Ecology and Vertebrate Zoology, Faculty LeBlanc 2007; Rooijakkers et  al. 2009), dolphins (Jaak- of Biology and Environmental Protection, University kola et al. 2010; Johnson et al. 2015), sea lions (Singer and of Lodz, Banacha 12/16, 90-237 Łódź, Poland Vol.:(0123456789) 1 3 604 Animal Cognition (2018) 21:603–611 Henderson 2015), dwarf goats (Nawroth et al. 2015), par- unintentional body language or gaze of the experimenter. rots (Pepperberg and Funk 1990), and corvids (Pollok et al. Associative learning might cause the animal to pass the 2000). Likewise, several species of monkey, such as long- test because they have learned simple associative rules tailed macaques (Schloegl et al. 2013), rhesus macaques such as ‘pick the location that the experimenter indicated’. (Filion et al. 1996) and cotton top tamarins (Neiworth et al. Although the Piagetian framework may have some limita- 2003), have become the subject of similar studies. Finally, tions, it is still very useful in examining and comparing great and lesser apes have also been examined (e.g. de Blois cognitive abilities of human and non-human animals (Pep- et al. 1998; Call 2003; Collier-Baker et al. 2006; Rooijakkers perberg 2002). et al. 2009; Anderson 2012). According to Amici et al. (2010), there is no overall Comparisons of the ability of object tracking have been clear-cut distinction in cognitive skills between apes and done in both non-human primates and children. Such com- monkeys, and existing differences have often been overes- parisons for infants and great apes have been carried out timated (Tomasello and Call 1997). However, due to mis- under varying degrees of difficulty (e.g. invisible and vis- cellaneous procedures applied in different experiments, it ible displacement). Findings have shown that children 19 is hard to make comparisons between species. For this rea- months, 2 years and 2.5 years old as well as great apes have son, we decided to apply the methods used by Rooijakkers very similar cognitive skills for dealing with the physical et al. (2009), who compared dogs and great apes in experi- world (Call 2001; Barth and Call 2006; Collier-Baker and ments on their ability to track visually object transposition. Suddendorf 2006; Herrmann et al. 2007). The purpose of this study was to investigate the ability According to Jaakkola’s (2014) classification, there are of some species of monkeys to track the displacement of three experimental methodologies to be applied for under- an object and to compare the results from the literature standing invisible displacement in non-human animals, on apes and dogs, to which the same method was applied namely, a Piagetian task, rotation and transposition. In a using the transposition task (Rooijakkers et al. 2009). In standard Piagetian task, the target object is hidden inside this study, we were also interested in evaluating how the the displacement device, which is subsequently placed under subjects solve problems depending on the level of a vari- one of three opaque containers. Next, the displacement ant’s complexity. device is removed and the experimenter shows the subject the empty device and then the subject starts to search for the object. In a rotation task, opaque containers are placed on a turntable. The experimenter places the target object under Methods one of the opaque containers and rotates the turntable (90° or 180°). The third type of task, transposition, requires that Ethical note the target object be placed directly in containers without the intermediate displacement device. Subsequently, one or The experiment was non-invasive, the subjects partici- two containers out of the two or three provided are moved. pated in it voluntarily and they were neither food nor water The way the cups are moved affects the level of difficulty of deprived for the testing. The study received the approval of the task. If the containers cross path or the empty container The Local Ethics Committee for Animal Experimentation moves into the initial position of the baited container, then (permit number 3/ŁB11/2016 of 18th January 2016) and it causes more difficulties for the subject to choose baited acted in accordance with the law from 15th January 2015 containers (Doré et al. 1996; Fiset and Plourde 2013; Jaak- on the protection of animals used for scientific purposes. kola 2014; Rooijakkers et al. 2009). In all three tasks (i.e. Piagetian, rotation, transposition), the subject possesses a mental representation of the situation and points by logical Subjects inference to the correct position of the target object invisibly moved (Jaakkola 2014). 19 monkeys (7 females and 12 males), born in captivity, To claim that a species understands invisible displace- participated in the experiment (Table  1). The monkeys ment, three factors must be controlled for or ruled out: were housed at zoos across Poland: in Łódź (six individu- sensory cues, social cues and associative learning. If these als), Warszawa (one individual), Wrocław (nine individu- factors are not controlled for, then they could affect the als) and Poznań (three individuals). All individuals lived results of experiments. Thanks to them, the animal could in indoor and outdoor enclosures, were fed their species- complete the task successfully without conceptual under- typical diet (vegetables, fruit, insects) and water was avail- standing of invisible displacement (Jaakkola 2014). Sen- able at all times. For all subjects, the experiment involved sory cues could be, e.g., smell in case of dogs or the abil- rewards hidden inside cups and transposition tasks were a ity to echolocate (cf. dolphins, bats). Social cues include new experience. 1 3 Animal Cognition (2018) 21:603–611 605 Table 1 Monkeys included in the experiment Subject (name) Species Sex Age (years) ZOO Cercopithecidae Old World Monkey  Grześ Pig-tailed macaque Macaca nemestrina (Linnaeus, 1766) Male 23 ZOO Łódź  Naomi Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Female 11 ZOO Łódź  Rani Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Female 21 ZOO Łódź  Woolfie Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Male 26 ZOO Łódź  Punio Lion-tailed macaque Macaca silenus (Linnaeus, 1758) Male 13 ZOO Łódź  Taro Celebes crested macaque Macaca nigra (Desmarest, 1822) Male 17 ZOO Wrocław  Tyson Barbary macaque Macaca sylvanus (Linnaeus, 1758) Male 11 ZOO Wrocław  Lisbeth Barbary macaque Macaca sylvanus (Linnaeus, 1758) Female 2 ZOO Wrocław  Ries Barbary macaque Macaca sylvanus (Linnaeus, 1758) Male 11 ZOO Wrocław  Canail Barbary macaque Macaca sylvanus (Linnaeus, 1758) Male 9 ZOO Wrocław  Hiszpan De Brazza’s monkey Cercopithecus neglectus Schlegel, 1876 Male 16 ZOO Łódź  Holly L’Hoest’s monkey Cercopithecus lhoesti Sclater, 1899 Female 8 ZOO Wrocław  Pyza Allen’s swamp monkey Allenopithecus nigroviridis (Pocock, 1907) Female 19 ZOO Warszawa  Corso Black crested mangabey Lophocebus aterrimus (Oudemans, 1890) Male 19 ZOO Wrocław  Alf Collared mangabey Cercocebus torquatus (Kerr, 1792) Male 16 ZOO Wrocław  Olaf Collared mangabey Cercocebus torquatus (Kerr, 1792) Male 5 ZOO Wrocław Atelidae New World Monkey  Zosia Geoffroy’s spider monkey Ateles geoffroyi Kuhl, 1820 Female 18 ZOO Poznań Zuza Geoffroy’s spider monkey Ateles geoffroyi Kuhl, 1820 Female 18 ZOO Poznań  Colombo Geoffroy’s spider monkey Ateles geoffroyi Kuhl, 1820 Male 17 ZOO Poznań the reward after choosing the correct cup. In the situation Warm‑up when the subject pointed to the un-baited cup, E1 showed an empty cup and where the reward is, but subject did not The monkeys were tested in the indoor or outdoor enclosures get it. The warm-up phase was completed when the subjects in which they lived. Enclosure selection depended on factors touched one of the two cups (baited or un-baited) five times. such as good visibility of the platform by the subject, not At this stage, the experimenter did not manipulate the cups finding any trace of the subject’s anxiety, and weather condi- in the same way as during the actual part of the experiment. tions. A wooden platform (60 × 30 cm) was attached outside of a mesh panel. There were four small dots on the platform Procedure at a distance of 15 cm from each other indicating the loca- tion of the cups. Two identical opaque grey cardboard cups The experiment always started in the same way. The for- (diameter 8 cm, 9 cm high) were used in the experiment. ward-facing experimenter (E1), invariably the same per- During the experiment, fruit and insects (species-typical son, sat in front of the subject, separated by the mesh panel diet) were provided as a reward. and the platform, and obtained its attention by showing All subjects underwent a warm-up phase prior to the the reward. Once the subject focused on the task, E1 put experiment with the aim to familiarise them with the pro- the food reward on the platform (location 2 or 4; Fig. 1) cedure of disappearance of food under cups and receiving it and next showed two empty cups and then covered the after touching the cup. The warm-up phase took place at the reward with one of them. The initial position of the cups same location where the experiment was later carried out in all variants was always the same (location 2 and 4). using the same platform and cups. The platform was fixed to After hiding the reward, the experimenter instantly pro- the net and left for 1 h to give the subjects time to get used to ceeded to manipulate the cups. E1 simultaneously moved it. The warm-up phase was conducted by the experimenter the cups from initial to final positions in the following (E1). During this phase, the cups were randomly distributed way: the right-hand side cup with his right-hand and the over the whole surface of the platform, but never in the loca- left-hand side cup with his left hand. After the cups were tions where they were to be presented during the experiment. put in their final positions (Fig.  1), the subject could touch E1 showed the empty cups to the subject and then covered either of them. It was only when the subject had made the the reward with one of the cups. The individual received 1 3 606 Animal Cognition (2018) 21:603–611 session, none of the variants could be repeated more than twice in a row. The variants were implemented as follows: Variant 1 E1 grabbed the right cup with the right hand and the left cup with the left hand, then with one continu- ous movement he moved the cups so that the cup from location 2 would be placed on location 1, and the cup from location 4 on location 3. Variant 2 E1 grabbed the right cup with the right hand and the left cup with the left hand, then with one continu- ous movement he moved the cups so that the cup from location 2 would be found on location 1, and the cup from location 4 on location 2. Variant 3 E1 grabbed the right cup with the right hand and the left cup with the left hand. Then with one con- tinuous motion, so that the arms would cross over the platform, moved the cup from location 2 to location 3, and the cup from location 4 to location 1. Variant 4 E1 grabbed the right cup with the right hand and the left cup with the left hand. Then with one con- tinuous motion, so that the arms would cross over the platform, moved the cup from location 2 to location 3, and the cup from location 4 to location 2. Variant 5 E1 grabbed the right cup with the right hand and the left cup with the left hand. Then with one con- tinuous motion, so that the arms would cross over the platform, moved the cup from location 2 to location 4, and the cup from location 4 to location 2 (Fig. 1). After completion of the experiments, a control test was Fig. 1 Schematic representation of the five different transposition var - performed in which the experimenter (E1) covered the cups iants performed in this study (according to Rooijakkers et  al. 2009). while placing the food to prevent the subject from knowing The grey cups represent the initial position, while the white ones indi- where it was hidden. The control procedure resembled the cate the final position in given variants if the cups were relocated. In experiment, but the monkey received the reward regardless all variants the start locations were the same. The order of the vari- ants presented by E1’s point of view: 2R, 5L, 1L, 3R, 4L, 5R, 1R, of the cup choice. The control test aimed at the exclusion of 3L, 4R, 2L, 2R, 5R, 1L, 3R, 4L, 5L, 1R, 3L, 4R, 2L (L, reward under such factors as the use of scent or unconscious hints given left–hand cup; R, reward under right-hand cup) by E1. The subjects entered the experiment voluntarily and could stop the experiment at any moment, departing from the place where it was carried out. Some subjects completed right choice that it received the hidden reward. The second the experiment during one session, whereas some subjects experimenter (E2), facing downwards, was present during lost interest in working with the experimenter. The experi- all trials, read out the subsequent numbers of the vari- ment was continued when the subject again approached the ants and noted whether the selection made by the subject place of the experiment. was correct or not. All the subjects underwent the experi- ment in the presence of five variants, each of them applied Data scoring and analysis four times, summing up to 20 trials total. Determined by drawing lots at the outset of the experiment, the order of Differences between variants were analysed by the ANOVA performing the random sequence of variants remained the Friedman test. In case of significant effects, a post hoc test same for each subject. The conditions of drawing lots stip- (Conover-Iman) was conducted. Second, the Wilcoxon test ulated that in each of the five task variants the food should was used to determine whether the results of the experiment be hidden twice under the right-hand side cup and twice in each variant were above chance. Third, differences (calcu- under the left-hand side one. What is more, during one lated separately for each variant) were investigated between 1 3 Animal Cognition (2018) 21:603–611 607 the results of the experiment and the control test using a non- Table 3 Results of post hoc Conover-Iman test comparing results of examined monkeys depends on variant of experiment (P value) parametric exact two-tailed statistic (Wilcoxon test). Finally, the findings obtained from the studied monkeys were com- Variant 1 Variant 2 Variant 3 Variant 4 Variant 5 pared with the raw scores of dogs and apes as available from Variant 1 the literature (Rooijakkers et al. 2009). To determine dif- Variant 2 0.285 ferences between dogs (N = 20) and monkeys (N = 19), and Variant 3 0.021 0.205 between apes (N = 8) and monkeys, the Mann–Whitney U Variant 4 0.002 0.030 0.349 test was performed separately for each variant. Variant 5 0.003 0.055 0.503 0.789 Significant values are highlighted in bold Results The individual results of the subjects tested in each variant examined monkeys performed above chance in all variants are shown in Table 2. (Wilcoxon test z > 2.65, P < 0.01 in all variants) (Fig. 2). When treated as a group, the subjects showed significant Differences between variants differences between the performance of the experiment to the result of the control test in each variant, which A significant effect of variant was observed (ANOVA excludes other external factors affecting selection of the Friedman test χ = 13.40, n = 19, df = 4, P < 0.01). Post cup during the test (Table 4). hoc Conover-Iman test showed that monkeys performed better in Variant 1, where both cups were moved to new locations without crossing each other’s path, compared Comparison of results with dogs and apes to Variants 3, 4 and 5, where cups crossed each other’s path. The subjects also achieved better results in Variant The monkeys subjected to the experiment achieved signifi- 2, where one cup moved to a new location and then substi- cantly better results than dogs (as reported in Rooijakkers tuted the initial location of the first without crossing each et al. 2009) in all five variants (Z > − 4.83, P ≤ 0.001 in all other’s path, compared to Variant 4 (Table 3). Overall, the cases Table 5; Fig. 2). However, the monkeys scored worse than apes (Rooijakkers et al. 2009) in Variant 2, 3, 4 and Table 2 Sum of correct choices Subjects Species Variant of each subject per variant (with four trials in each variant) 1 2 3 4 5 Grześ Pig-tailed macaque 3 3 3 2 4 Naomi Lion-tailed macaque 4 4 4 4 4 Rani Lion-tailed macaque 4 3 2 2 3 Woolfie Lion-tailed macaque 3 3 3 4 3 Punio Lion-tailed macaque 4 3 3 2 1 Taro Celebes crested macaque 3 3 3 3 4 Tyson Barbary macaque 3 4 3 4 3 Canail Barbary macaque 4 4 4 4 3 Ries Barbary macaque 4 3 4 4 4 Lisbeth Barbary macaque 4 3 2 2 3 Hiszpan De Brazza’s monkey 4 4 4 1 3 Holly L’Hoest’s monkey 4 4 4 2 2 Pyza Allen’s swamp monkey 4 3 2 2 2 Corso Black crested mangabey 4 3 4 4 3 Alf Collared mangabey 4 4 4 4 3 Olaf Collared mangabey 4 4 3 4 4 Zosia Geoffroy’s spider monkey 4 4 3 2 2 Zuza Geoffroy’s spider monkey 4 4 3 2 3 Colombo Geoffroy’s spider monkey 3 3 3 2 3 1 3 608 Animal Cognition (2018) 21:603–611 a, b a, b a, b Fig. 2 Mean number (± SEM) a a, b of correct response of the monkeys (N = 19) in the current study and the dogs (N = 20) and monkeys the apes (N = 8) from Rooijak- apes* kers et al. (2009) for each of the five variants. Statistically dogs* significant differences between the dogs and the monkeys (P < 0.01). statistically sig- nificant differences between the monkeys and the apes (P < 0.05) CHANCE Variant 1Variant 2Variant 3Variant 4Variant 5 * -Rooijakkerset al. (2009) Table 4 Wilcoxon test results subjects to track the position and find the hidden reward T z P comparing the performance of if the cups did not cross each other’s path during move- the subjects to the result of the Variant 1 0 3.62 < 0.001 ments. In fact, the monkeys obtained worse results if the control test Variant 2 0 3.62 < 0.001 paths of the two cups were crossed and the two containers Variant 3 9 3.05 0.01 exchanged locations with one another. Although monkeys Variant 4 5 2.67 0.01 performed above chance level in all variants, they scored Variant 5 15 2.13 0.03 significantly worse than the apes examined by Rooijakkers et al. (2009), except for Variant 1. In the latter experiment, which employed exactly the same procedure of this study, chimpanzees, bonobos, orangutans and gorillas succeeded 5. It was only in Variant 1 that no statistically significant differences were noted (Table  5; Fig. 2). in all variants, and the level of difficulty did not affect the results of the apes (Rooijakkers et al. 2009). In another experiment using a Piagetian task, which involved object transposition in the presence of the above-mentioned ape Discussion species, all subjects selected the correct cup above chance level and there were no significant differences amongst In the present study using the transposition task, monkeys were successful in all variants, both in the case of a sim- single and double (the reward changed the position twice) displacement tasks (Barth and Call 2006). Call (2001) ple displacement of the two cups and in displacements with reverse swapping. However, there were differences observed that orangutans, chimpanzees and 26-month- old children performed above chance level on visible in the number of correct choices according to the level of a variant’s complexity. Generally, it was easier for the and invisible displacement tasks, except for nonadjacent Table 5 Comparison of Comparison Monkeys Apes Dogs Monkeys/dogs Monkeys/apes the results of the examined monkeys and dogs and the Mean (± SD) Mean (± SD) Mean (± SD) Z P Z P results of monkeys and apes Variant 1 3.74 (± 0.45) 4.00 (± 0.00) 2.85 (± 0.88) − 3.23 0.001 1.54 0.12 [data on dogs and apes from Rooijakkers et al. (2009)] Variant 2 3.47 (± 0.51) 4.00 (± 0.00) 2.30 (± 1.08) − 3.57 < 0.001 2.51 0.01 (Mann–Whitney U test) Variant 3 3.21 (± 0.71) 3.88 (± 0.35) 1.85 (± 0.59) − 4.59 < 0.001 2.33 0.02 Variant 4 2.84 (± 1.07) 3.75 (± 0.46) 1.65 (± 0.81) − 3.21 0.001 2.02 0.04 Variant 5 3.00 (± 0.82) 3.63 (± 1.06) 1.00 (± 0.92) − 4.83 < 0.001 2.26 0.02 1 3 Animal Cognition (2018) 21:603–611 609 invisible displacements (i.e. the reward was moved to a social world. In nature, apes are forced to gain food from nonadjacent container). In another of Call’s (2003) experi- hidden locations (e.g. underground nests), which requires ments, several tasks were presented to chimpanzees and causal understanding, and sometimes they need to use a tool. orangutans. In the no-landmark transposition (food is pre- Probably because of this, they have evolved to develop skills sented directly to the subject), apes performed better than in reading causal cues (Bräuer et al. 2006). in the landmark (the subject had to infer the position of Dogs are considered to have an ability to read human the reward using a landmark) transposition test, whereas behaviour and use triadic communication, i.e. one individ- in the latter subjects obtained significantly better results in ual informs another about the location of various things, the no-swap transposition compared to the reverse swap. including food resources, for example, by pointing or other Overall, the results obtained by monkeys vary among gestures. Their skills in understanding cooperative signs experiments using a Piagetian task. For instance, long- have developed over thousands of years of domestication tailed macaques performed above chance level in single (Coppinger and Coppinger 2002; Hare and Tomasello 2005; and double transpositions (Amici et al. 2010), spider mon- Bräuer et al. 2006). On the other hand, as a result of domesti- keys only in a single transposition, but neither coped with cation, dogs could have lost some skills necessary for causal a reverse transposition, that is, when the baited cup and understanding due to lack of subsistence problems thanks to empty cup switched location twice and returned to their humans (Bräuer et al. 2006; Rooijakkers et al. 2009; Wynne original position. Experiments on cotton top tamarins 2016). Furthermore, ontogenetic development of interspe- revealed that their performance was above chance level cies cooperative skills in a dog may well result from the in both visible and invisible displacement tasks and only relationship established with a human in the first weeks of in one (i.e. double invisible displacement with the second its life, which is usually not the case with primates subjected cup manipulated by the experimenter) did results dropped to experiments (Miklósi et al. 2003; Wynne et al. 2008). to chance level (Neiworth et al. 2003). Even though the According to the hypothesis of Natale et al. (1986), mon- procedures adopted in the aforementioned experiments keys’ progress is limited to Stage 5 on the Piagetian scale differed, it is certain that a transposition which comprises of sensorimotor development of object permanence. The crossing paths poses difficulty to many species of pri- authors of that study presumed that only apes, hence not mates. It is solely apes that tackled such tasks successfully monkeys, could solve a task with the use of mental repre- regardless of difficulty level. sentation. However, the results of the present experiments as The monkeys used in the present experiment scored well as those of other researchers have given evidence for the significantly better in all tasks than the dogs examined by reaching of Stage 6 by the examined monkeys. The species Rooijakkers et al. (2009), which performed above chance of monkeys that demonstrated good cognitive abilities is the only in Condition 1 (i.e. both containers moved to a new cotton top tamarin, and results have shown that they possess location and not crossing each other’s path). If the containers Stage 6 object permanence (Neiworth et al. 2003). On the changed their position in such a way that they crossed each other hand, another monkey species, namely, the squirrel other’s path, then the dogs could not follow the transition monkey, did not possess this stage (de Blois et al. 1998). of the reward. This seems to indicate that monkeys exhibit Amongst primates, it was only lemurs that demonstrated more flexibility in mental representation compared to dogs. Stage 5 of object permanence, as they failed in invisible dis- Rooijakkers et al. (2009) assumed that great apes use their placement tasks—a result explained by Deppe et al. (2009) mental representation more flexibly than dogs. Undoubt- to be of ecological relevance. According to their hypothesis, edly, one must also concur with Rooijakkers et al. (2009), lemurs’ ability to obtain stationary fruit or leaves and to who noted that dog inferential abilities are better expressed avoid predators such as raptors, snakes and viverrids does in the olfactory than in the visual modality. Moreover, dif- not have to go beyond solving a visible displacement task. ferences in cognitive abilities between dogs and primates Lemurs are attacked by fossas, a large cat-like carnivore in are well illustrated by Bräuer et al.’s (2006) research. Their Madagascar, only during sleep. Snakes hunt them using sit- experiments showed that dogs perform better at finding hid- and-wait tactics, whereas raptors observed through foliage den food using communicative cues given by the human can appear in and disappear from the field of view (Good- experimenter, whereas apes do better when the reward man 2003). On the other hand, in animals which are at risk causes a noticeable change in the physical world (e.g. by of attack by terrestrial stalking predators such as felines, generating a noise). Generally, the cup manipulated by the possessing Stage 6 object permanence is very important experimenter was preferred by the examined dogs and they (Deppe et al. 2009). achieved almost 50% better results than the apes in under- In the case of non-primate animals, some species standing communicative cues (Bräuer et al. 2006). The latter of birds can achieve a high level of cognitive abilities. experiment provided arguments for apes’ developed ability Four species of parrots (i.e. an African Grey parrot, an to make inferences about the working of the physical and Illiger macaw, a cockatiel, and a parakeet) showed Stage 1 3 610 Animal Cognition (2018) 21:603–611 credit to the original author(s) and the source, provide a link to the 6 competence (Pepperberg and Funk 1990), and this level Creative Commons license, and indicate if changes were made. was also achieved by Eurasian jays (Zucca et al. 2007). Zucca et al. (2007) concluded that a Stage 5 competence would suffice for those birds to collect food, even though it is not enough for protecting their caches of food. Suc- References cessful protection of food is probably associated with the understanding of intentions and the manipulation of poten- Amici F, Aureli F, Call J (2010) Monkeys and apes: are their tial pilferers (Clayton and Dickinson 1998). cognitive skills really so different? Am J Phys Anthropol The human brain was designed by natural selection to 143:188–197 Anderson MR (2012) Comprehension of object permanence and sin- solve adaptive problems faced by our hunter–gatherer ances- gle transposition in gibbons. Behaviour 149:441–459. https :// tors (Duchaine et al. 2001). Obviously, the same process can doi.org/10.1163/15685 3912X 63976 9 be observed by examining the brain and adaptations in non- Barth J, Call J (2006) Tracking the displacement of objects: a series human species. The importance of cross-species compari- of tasks with great apes (Pan troglodytes, Pan paniscus. Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapi- sons to test evolutionary functions of organismic design is ens). J Exp Psychol Anim Behav Process 32(3):239–252 highly emphasised by evolutionary biologists, comparative Bräuer J, Kaminski J, Riedel J, Call J, Tomasello M (2006) Making psychologists, and behavioural ecologists. In this respect, inferences about the location of hidden food: social dog, causal an analysis of results regarding cognitive traits showed that ape. J Comp Psychol 120(1):38–47 Call J (2001) Object Permanence in Orangutans (Pongo pygmaeus), they probably evolved independently amongst several ver- Chimpanzees (Pan troglodytes), and Children (Homo sapiens). tebrate groups including Primates (Reader et al. 2011; van J Comp Psychol 115(2):159–171 Horik et al. 2012). The results of the examined species of Call J (2003) Spatial rotations and transpositions in orangutans monkeys, as well as data from the literature on corvids, par- (Pongo pygmaeus) and chimpanzees (Pan troglodytes). Primates 44:347–357 rots, cetaceans, and apes, showed that the understanding of Clayton NS, Dickinson A (1998) Episodic-like memory during cache object permanence in such species is at a similar stage of recovery by scrub jays. Nature 395:272–278 development (Stage 6 competence). According to van Horik Collier-Baker E, Suddendorf T (2006) Do Chimpanzees (Pan trog- et al.’s (2012) hypothesis, cognitive traits might have arisen lodytes) and 2-year-old children (Homo sapiens) understand double invisible displacement? J Comp Psychol 120(2):89–97 in distantly related groups (e.g. corvids and apes) because Collier-Baker E, Davis JM, Nielsen M, Suddendorf T (2006) Do they have evolved to solve similar environmental problems. chimpanzees (Pan troglodytes) understand single invisible dis- Having analysed many biological, ecological, behavioural placement? Anim Cogn 9:55–61 and social system traits, the authors of that study conclude Coppinger R, Coppinger L (2002) Dogs: a new understanding of canine origin, behaviour and evolution. Chicago University that, despite having different brain structures, there are strik - Press, Chicago ing similarities in the diet, use of tools, and social systems in de Blois ST, Novak MA, Bond M (1998) Object permanence in corvids, parrots, apes, cetaceans, and elephants. Van Horik Orangutans (Pongo pygmaeus) and Squirrel Monkeys (Saimiri et al.’s (2012) study also speculated that species character- sciureus). J Comp Psychol 112(2):137–152 Deppe AM, Patricia C, Wright PC, Szelistowski WA (2009) Object ised by a relatively large brain and that undergo a long devel- permanence in lemurs. Anim Cogn 12:381–388 opmental period, that live a long life and live in a fluctuating Doré FY, Fiset S, Goulet S, Dumas MC, Gagnon S (1996) Search habitat, could all be considered candidates for convergent behavior in cats and dogs: interspecific differences in working evolution of cognitive abilities. It is, therefore, believed that memory and spatial cognition. Anim Learn Behav 24:142–149. https ://doi.org/10.3758/BF031 98962 the monkeys studied in the present experiment match well Duchaine B, Cosmides L, Tooby J (2001) Evolutionary psychology with the aforementioned groups of vertebrates. Finally, it is and the brain. Curr Opin Neurobiol 11:225–230 worthwhile to investigate further the cognitive abilities of Filion CM, Washburn DA, Gulledge JP (1996) Can monkeys other, hitherto not yet examined species, and particularly (Macaca mulatta) represent invisible displacement? J Comp Psychol 110(4):386–395 monkeys, because some major advances in our understand- Fiset S, LeBlanc V (2007) Invisible displacement understanding ing of evolution have resulted from a convergence of data in domestic dogs (Canis familiaris): the role of visual cues in from numerous species (Sell 2012). search behaviour. Anim Cogn 10:211–224 Fiset S, Plourde V (2013) Object permanence in domestic dogs Acknowledgements We sincerely thank the Lodz ZOO, the Warsaw (Canis lupus familiaris) and gray wolves (Canis lupus). J Comp ZOO, the Poznan ZOO and the Wroclaw ZOO for allowing us to con- Psychol 127:115–127. https ://doi.org/10.1037/a0030 595 duct the experiments. We wish to thank the staff for their cooperation Goodman SM (2003) Predation on lemurs. In: Goodman SM, Ben- and patience during this project. stead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1221–1228 Hare B, Tomasello M (2005) Human-like social skills in dogs? Open Access This article is distributed under the terms of the Crea- Trends Cogn Sci 9:439–444 tive Commons Attribution 4.0 International License (http://creat iveco Herrmann E, Call J, Hernández-Lloreda MV, Hare B, Tomasello mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- M (2007) Humans have evolved specialized skills of social tion, and reproduction in any medium, provided you give appropriate 1 3 Animal Cognition (2018) 21:603–611 611 cognition: the cultural intelligence hypothesis. Science Piaget J (1954) The construction of reality in the child. Basic Books, 317:1360–1366 New York Horik JO, Clayton NS, Emery NJ (2012) Convergent evolution of Pollok B, Prior H, Güntürkün O (2000) Development of object per- cognition in corvids, apes and other animals. In Shackelford TK, manence in food-storing magpies (Pica pica). J Comp Psychol Vonk J (eds), The Oxford handbook of comparative evolution- 114(2):148–157 ary psychology. The Oxford University Press, Oxford Reader SM, Hager Y, Laland KN (2011) The evolution of pri- Jaakkola K (2014) Do animals understand invisible displacement? A mate general and cultural intelligence. Philos Trans R Soc B critical review. J Comp Psychol 128(3):225–239 366:1017–1027 Jaakkola K, Guarino E, Rodriguez M, Erb L, Trone M (2010) What Rooijakkers EF, Kaminski J, Call J (2009) Comparing dogs and great do dolphins (Tursiops truncatus) understand about hidden apes in their ability to visually track object transpositions. Anim objects? Anim Cogn 13:103–120 Cogn 12:789–796 Johnson CM, Sullivan J, Buck CL, Trexel J, Scarpuzzi M (2015) Vis- Schloegl C, Waldmann MR, Fischer J (2013) Understanding of and rea- ible and invisible displacement with dynamic visual occlusion soning about object–object relationships in long-tailed macaques? in bottlenose dolphins (Tursiops spp). Anim Cogn 18:179–193 Anim Cogn 16:493–507 Miklósi A, Kubinyi E, Topál J, Gácsi M, Virányi Z, Csányi V (2003) Sell AN (2012) Evolved cognitive adaptations. In: Shackelford TK, A simple reason for a big difference: wolves do not look back at Vonk J (eds) The Oxford handbook of comparative evolutionary humans, but dogs do. Curr Biol 13:763–766 psychology. The Oxford University Press, Oxford Natale F, Antinucci F, Spinozzi G, Poti P (1986) Stage 6 object concept Shreve KRV, Udel MAR (2015) What’s inside your cat’s head? A in nonhuman primate cognition: a comparison between Gorilla review of cat (Felis silvestris catus) cognition research past, pre- (Gorilla gorilla gorilla) and Japanese Macaque (Macaca fuscata). sent and future. Anim Cogn 18:1195–1206 J Comp Psychol 100(4):335–339 Singer R, Henderson E (2015) Object permanence in marine mam- Nawroth C, von Borell E, Langbein J (2015) Object permanence in the mals using the violation of expectation procedure. Behav Proc dwarf goat (Capra aegagrus hircus): perseveration errors and the 112:108–113 tracking of complex movements of hidden objects. Appl Anim Tomasello M, Call J (1997) Primate cognition. Oxford University Behav Sci 167:20–26 Press, New York Neiworth JJ, Steinmark E, Basile BM, Wonders R, Steely F, DeHart C Wynne CDL (2016) What is special about dog cognition? Curr Dir (2003) A test of object permanence in a new-world monkey spe- Psychol Sci 25(5):345–351 cies, cotton top tamarins (Saguinus oedipus). Anim Cogn 6:27–37 Wynne CDL, Udell MAR, Lord KA (2008) Ontogeny’s impacts on Pepperberg IM (2002) The value of the Piagetian framework for com- human-dog communication. Anim Behav 76:e1–e4. https ://doi. parative cognitive studies. Anim Cogn 5:177–182org/10.1016/j.anbeh av.2008.03.010 Pepperberg IM, Funk MS (1990) Object permanence in four species Zucca P, Milos N, Vallortigara G (2007) Piagetian object permanence of psittacine birds: an African Grey parrot (Psittacus erithacus), and its development in Eurasian jays (Garrulus glandarius). Anim an Illiger mini macaw (Ara maracana), a parakeet (Melopsittacus Cogn 10:243–258 undulatus), and a cockatiel (Nymphicus hollandicus). Anim Learn Behav 18(1):97–108 1 3

Journal

Animal CognitionSpringer Journals

Published: Jun 1, 2018

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off