Misinterpreting “cost” in the classification of animal teaching

Misinterpreting “cost” in the classification of animal teaching A recent article by Kleindorfer et al. (2014) has made a strong case for animal teaching in superb fairy wrens (Malurus cyaneus). The article built upon a previous experiment showing that fairy-wren incubation calling met 2 criteria in the Caro and Hauser (1992) functional definition of animal teaching. Wrens sang an unique call—an incubation call—only to their embryonic young (Criterion 1), and those young learned the song better than young without such demonstration, allowing mothers to later distinguish wrens from cuckoo chicks (Criterion 3) (Colombelli-Négrel et al. 2012). The 2014 article showed that incubation calling in the wild was correlated with the cost of increased predation on eggs. Also, experimental broadcasting of incubation calls attracted predators and increased predation on eggs compared to no-call controls. The main claim of the study was that incubation calling was an example of animal teaching because calling was costly to the parent (Criterion 2). However, the article has misinterpreted the functional definition of cost in animal teaching described by Caro and Hauser (1992). Caro and Hauser’s seminal article implied that the cost of teaching must be personal and immediate. One example of cost from Caro and Hauser (1992) was the cheetah “that taught its young to disable prey prolonged the time until eating and expended effort in chasing prey”; another example was that releasing prey for cubs increased the chance of prey escaping and parents would have to rehunt the prey. The purpose of measuring these immediate personal costs is to ensure that parents’ putative teaching behavior is not immediately self-serving (Thornton and Raihani 2008). This is because teaching is typically defined as cooperative—immediately costly or of no benefit to the teacher, beneficial to the pupil, and beneficial to both in the long-term (West et al. 2007). Thus the standard method to operationalize teaching as cooperative is by testing immediate personal costs to the parent (Thornton and Raihani 2010), as shown in Table 1. Note that the functional definition is satisfied even without cost, as long as the teacher gains no immediate benefit from teaching. This inductive method, to hypothesize various potential benefits that the animal might gain and then disprove them, is accepted as one useful way of showing that putative teaching is cooperative (Thornton and Raihani 2010; Thornton and McAuliffe 2012). Yet cost is a more powerful, deductively logical way of showing that teaching is cooperative. Cost is clearly favored in the literature, and is thus important to clarify within the functional definition of animal teaching. Table 1 Cost as defined in some well-established examples of animal teaching Species  Candidate teaching behavior  Proposed cost: opportunity and energy cost  Ants  In ant tandum-running pairs, leader ants modify their speed and course depending on the follower. The follower learns the route to food faster as a result.  The leader ants in tandem-running pairs take 4 times longer to reach food compared to when walking alone.  Bees  Knowledgeable workers waggle-dance to indicate the typical locations and characteristics of food.  The bee that dances competes with more bees for food and waits longer until the next foraging opportunity.  Meerkats and cheetahs  Parents catch and maim prey and provide the disabled prey to offspring, which become more comfortable with the prey.  Parents risk that the offspring will allow the prey to escape and that they will have to rehunt the prey.  Species  Candidate teaching behavior  Proposed cost: opportunity and energy cost  Ants  In ant tandum-running pairs, leader ants modify their speed and course depending on the follower. The follower learns the route to food faster as a result.  The leader ants in tandem-running pairs take 4 times longer to reach food compared to when walking alone.  Bees  Knowledgeable workers waggle-dance to indicate the typical locations and characteristics of food.  The bee that dances competes with more bees for food and waits longer until the next foraging opportunity.  Meerkats and cheetahs  Parents catch and maim prey and provide the disabled prey to offspring, which become more comfortable with the prey.  Parents risk that the offspring will allow the prey to escape and that they will have to rehunt the prey.  View Large However, in the article by Kleindorfer et al. (2014), “predation cost” referred to an increased risk of death incurred by the pupil, not the parent. Immediate, personal costs to the parent remained untested. Certainly, “predation cost” reduced the mother’s chances of reproducing her genes, but this harm was in the long term and not necessarily in the immediate sense. Studying the balance of long-term evolutionary costs and benefits to the teacher is highly important to understand why teaching exists, but not if teaching exists (Thornton and Raihani 2008). Only immediate, personal costs allow us to deduce whether or not incubation calling was immediately self-serving because any immediately costly teaching would be unappealing to an animal acting purely from self-interest rather than cooperatively. Therefore, “predation cost” hindered the authors from showing that incubation calling meets the functional definition of animal teaching. Despite this, the fairy wren study remains a strong case for teaching, and mother wrens surely do incur some kind of immediate personal costs for incubation calling. First, predation cost may be not only a long-term cost (offspring dying) but also a personal cost to the parent that varies the frequency of incubation calling, although this distinction was not discussed. Second, the mother may undergo a different personal cost for incubation calling, such as increased risk of a predator attacking the mother as suggested by Raihani and Ridley (2008). Or third, it is likely that calling demands significant energy. Indeed, a similar study in pied babblers showed that mother babblers expended significant energy in calling to their babies as measured by weight loss (Raihani and Ridley 2008). Singing for an hour is hard work! Nonetheless it is important to illustrate that the study—though intending to follow Caro and Hauser’s functional definition of teaching closely—did not interpret the definition of cost in the spirit of what teaching actually is, a cooperative behavior. Another recent study on chimpanzees did assess immediate personal costs to the teacher but has functionally defined teaching in a suboptimal way by focusing purely on opportunity costs. In the study, Musgrave et al. (2016) hypothesized that tool transfer from parent to offspring chimpanzee was a form of opportunity teaching that helped offspring learn to probe for termites in termite-mounds. They found that the duration of termite fishing, the number of probes into the termite mound, and the number of “feeding events” all decreased for the parent putative teacher and increased for the offspring. Yet, these “costs” seem small compared to the standard in the literature, where costs are generally one of either: 1) Extra time lost, 2) Lost investments, 3) Danger, or 4) Energy (Thornton and Raihani 2010). For example, unlike the cheetahs that risk having to rehunt the prey they gave their young (lost investment), these chimp parents bore no risk of losing tools or termites. Also, the parents apparently expended no significant energy in tool transfer, because they simply handed the young a tool then watched or continued probing with their own tool. Rather, the costs measured seem to be opportunity costs only. That is, after the tool transfer, the parent chimpanzees spent some of the time they would normally be probing for termites just sitting and watching. Even then, the parents did not forego their meal entirely—in none of the tool transfers did parents not eat—meaning that the lost opportunity was not eating termites, but eating more termites. Indeed, the parents often prepared for tool transfer by bringing a spare tool or splitting their tool in 2 (which takes a split-second, see their Supplementary video). The authors argued that parents bore a cost by preparing for tool transfer. Conversely, preparing for tool transfer suggests that at the time of tool transfer parents were not greatly hindered by the tool transfer compared to the benefits they would accrue, such as less harassment. These opportunity costs to chimp parents were immediate and personal to the parent, and may suggest the parents acted cooperatively. However, as evidence of cost they are certainly in a weaker category compared to all other serious examples of animal teaching, in which parents bear serious energy costs for teaching (see Table 1. e.g., Leader ants walk 4 times as long as usual). For example, in the pied babbler study the authors mention that opportunity costs like missed foraging and preening may be relevant, but proceed to measure more substantive costs such as energy expenditure. All behavior, even self-interested behavior, comes at some opportunity cost. Thus, it seems that the onus is on animal researchers to show that a missed opportunity would have been more personally beneficial than putative teaching. Whereas this study of chimpanzees technically satisfies Criterion 2 of animal teaching, it is important to qualify the results by understanding that the grade of cost was lower for parent chimpanzees than in other examples of teaching. As argued by Byrne and Rapaport (2011), these two studies certainly have contributed valuably to the field of animal teaching. However, I echo the concerns of Thornton and McAuliffe (2012) that researchers in this growing field must strive for high quality knowledge. That means clarifying—if not necessarily adhering to word for word—the nuances of the functional definition of teaching. In this essay I have aimed to clarify the purpose of cost in defining animal teaching. The fairy wren study has shown that we ought to functionally define cost as immediate and personal to the teacher, so to ensure that the putative teaching is cooperative. Furthermore, the chimpanzee study has highlighted the various grades of costs, and particularly that opportunity costs are less convincing than energy costs in deciding whether putative teachers are acting cooperatively rather than merely out of self-interest. I hope that future research can now benefit from a clearer understanding of the nuances of cost in animal teaching. The author thanks Professor Justin Harris and Dr. Mike Kendig for their support. REFERENCES Byrne RW, Rapaport LG. 2011. What are we learning from teaching? Anim Behav . 82: 1207– 1211. Google Scholar CrossRef Search ADS   Caro TM, Hauser MD. 1992. Is there teaching in nonhuman animals? Q Rev Biol . 67: 151– 174. Google Scholar CrossRef Search ADS PubMed  Colombelli-Négrel D, Hauber ME, Robertson J, Sulloway FJ, Hoi H, Griggio M, Kleindorfer S. 2012. Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr Biol . 22: 2155– 2160. Google Scholar CrossRef Search ADS PubMed  Kleindorfer S, Hoi H, Evans C, Mahr K, Robertson J, Hauber ME, Colombelli-Négrel D. 2014. The cost of teaching embryos in superb fairy-wrens. Behav Ecol . 25: 1131– 1135. Google Scholar CrossRef Search ADS   Musgrave S, Morgan D, Lonsdorf E, Mundry R, Sanz C. 2016. Tool transfers are a form of teaching among chimpanzees. Sci Rep . 6: 34783. Google Scholar CrossRef Search ADS PubMed  Raihani NJ, Ridley AR. 2008. Experimental evidence for teaching in wild pied babblers. Anim Behav . 75: 3– 11. Google Scholar CrossRef Search ADS   Thornton A, McAuliffe K. 2012. Teaching can teach us a lot. Anim Behav . 83: e6–e9. Thornton A, Raihani NJ. 2008. The evolution of teaching. Anim Behav . 75: 1823– 1836. Google Scholar CrossRef Search ADS   Thornton A, Raihani NJ. 2010. Identifying teaching in wild animals. Learn Behav . 38: 297– 309. Google Scholar CrossRef Search ADS PubMed  West SA, Griffin AS, Gardner A. 2007. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol . 20: 415– 432. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Misinterpreting “cost” in the classification of animal teaching

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© The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
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Abstract

A recent article by Kleindorfer et al. (2014) has made a strong case for animal teaching in superb fairy wrens (Malurus cyaneus). The article built upon a previous experiment showing that fairy-wren incubation calling met 2 criteria in the Caro and Hauser (1992) functional definition of animal teaching. Wrens sang an unique call—an incubation call—only to their embryonic young (Criterion 1), and those young learned the song better than young without such demonstration, allowing mothers to later distinguish wrens from cuckoo chicks (Criterion 3) (Colombelli-Négrel et al. 2012). The 2014 article showed that incubation calling in the wild was correlated with the cost of increased predation on eggs. Also, experimental broadcasting of incubation calls attracted predators and increased predation on eggs compared to no-call controls. The main claim of the study was that incubation calling was an example of animal teaching because calling was costly to the parent (Criterion 2). However, the article has misinterpreted the functional definition of cost in animal teaching described by Caro and Hauser (1992). Caro and Hauser’s seminal article implied that the cost of teaching must be personal and immediate. One example of cost from Caro and Hauser (1992) was the cheetah “that taught its young to disable prey prolonged the time until eating and expended effort in chasing prey”; another example was that releasing prey for cubs increased the chance of prey escaping and parents would have to rehunt the prey. The purpose of measuring these immediate personal costs is to ensure that parents’ putative teaching behavior is not immediately self-serving (Thornton and Raihani 2008). This is because teaching is typically defined as cooperative—immediately costly or of no benefit to the teacher, beneficial to the pupil, and beneficial to both in the long-term (West et al. 2007). Thus the standard method to operationalize teaching as cooperative is by testing immediate personal costs to the parent (Thornton and Raihani 2010), as shown in Table 1. Note that the functional definition is satisfied even without cost, as long as the teacher gains no immediate benefit from teaching. This inductive method, to hypothesize various potential benefits that the animal might gain and then disprove them, is accepted as one useful way of showing that putative teaching is cooperative (Thornton and Raihani 2010; Thornton and McAuliffe 2012). Yet cost is a more powerful, deductively logical way of showing that teaching is cooperative. Cost is clearly favored in the literature, and is thus important to clarify within the functional definition of animal teaching. Table 1 Cost as defined in some well-established examples of animal teaching Species  Candidate teaching behavior  Proposed cost: opportunity and energy cost  Ants  In ant tandum-running pairs, leader ants modify their speed and course depending on the follower. The follower learns the route to food faster as a result.  The leader ants in tandem-running pairs take 4 times longer to reach food compared to when walking alone.  Bees  Knowledgeable workers waggle-dance to indicate the typical locations and characteristics of food.  The bee that dances competes with more bees for food and waits longer until the next foraging opportunity.  Meerkats and cheetahs  Parents catch and maim prey and provide the disabled prey to offspring, which become more comfortable with the prey.  Parents risk that the offspring will allow the prey to escape and that they will have to rehunt the prey.  Species  Candidate teaching behavior  Proposed cost: opportunity and energy cost  Ants  In ant tandum-running pairs, leader ants modify their speed and course depending on the follower. The follower learns the route to food faster as a result.  The leader ants in tandem-running pairs take 4 times longer to reach food compared to when walking alone.  Bees  Knowledgeable workers waggle-dance to indicate the typical locations and characteristics of food.  The bee that dances competes with more bees for food and waits longer until the next foraging opportunity.  Meerkats and cheetahs  Parents catch and maim prey and provide the disabled prey to offspring, which become more comfortable with the prey.  Parents risk that the offspring will allow the prey to escape and that they will have to rehunt the prey.  View Large However, in the article by Kleindorfer et al. (2014), “predation cost” referred to an increased risk of death incurred by the pupil, not the parent. Immediate, personal costs to the parent remained untested. Certainly, “predation cost” reduced the mother’s chances of reproducing her genes, but this harm was in the long term and not necessarily in the immediate sense. Studying the balance of long-term evolutionary costs and benefits to the teacher is highly important to understand why teaching exists, but not if teaching exists (Thornton and Raihani 2008). Only immediate, personal costs allow us to deduce whether or not incubation calling was immediately self-serving because any immediately costly teaching would be unappealing to an animal acting purely from self-interest rather than cooperatively. Therefore, “predation cost” hindered the authors from showing that incubation calling meets the functional definition of animal teaching. Despite this, the fairy wren study remains a strong case for teaching, and mother wrens surely do incur some kind of immediate personal costs for incubation calling. First, predation cost may be not only a long-term cost (offspring dying) but also a personal cost to the parent that varies the frequency of incubation calling, although this distinction was not discussed. Second, the mother may undergo a different personal cost for incubation calling, such as increased risk of a predator attacking the mother as suggested by Raihani and Ridley (2008). Or third, it is likely that calling demands significant energy. Indeed, a similar study in pied babblers showed that mother babblers expended significant energy in calling to their babies as measured by weight loss (Raihani and Ridley 2008). Singing for an hour is hard work! Nonetheless it is important to illustrate that the study—though intending to follow Caro and Hauser’s functional definition of teaching closely—did not interpret the definition of cost in the spirit of what teaching actually is, a cooperative behavior. Another recent study on chimpanzees did assess immediate personal costs to the teacher but has functionally defined teaching in a suboptimal way by focusing purely on opportunity costs. In the study, Musgrave et al. (2016) hypothesized that tool transfer from parent to offspring chimpanzee was a form of opportunity teaching that helped offspring learn to probe for termites in termite-mounds. They found that the duration of termite fishing, the number of probes into the termite mound, and the number of “feeding events” all decreased for the parent putative teacher and increased for the offspring. Yet, these “costs” seem small compared to the standard in the literature, where costs are generally one of either: 1) Extra time lost, 2) Lost investments, 3) Danger, or 4) Energy (Thornton and Raihani 2010). For example, unlike the cheetahs that risk having to rehunt the prey they gave their young (lost investment), these chimp parents bore no risk of losing tools or termites. Also, the parents apparently expended no significant energy in tool transfer, because they simply handed the young a tool then watched or continued probing with their own tool. Rather, the costs measured seem to be opportunity costs only. That is, after the tool transfer, the parent chimpanzees spent some of the time they would normally be probing for termites just sitting and watching. Even then, the parents did not forego their meal entirely—in none of the tool transfers did parents not eat—meaning that the lost opportunity was not eating termites, but eating more termites. Indeed, the parents often prepared for tool transfer by bringing a spare tool or splitting their tool in 2 (which takes a split-second, see their Supplementary video). The authors argued that parents bore a cost by preparing for tool transfer. Conversely, preparing for tool transfer suggests that at the time of tool transfer parents were not greatly hindered by the tool transfer compared to the benefits they would accrue, such as less harassment. These opportunity costs to chimp parents were immediate and personal to the parent, and may suggest the parents acted cooperatively. However, as evidence of cost they are certainly in a weaker category compared to all other serious examples of animal teaching, in which parents bear serious energy costs for teaching (see Table 1. e.g., Leader ants walk 4 times as long as usual). For example, in the pied babbler study the authors mention that opportunity costs like missed foraging and preening may be relevant, but proceed to measure more substantive costs such as energy expenditure. All behavior, even self-interested behavior, comes at some opportunity cost. Thus, it seems that the onus is on animal researchers to show that a missed opportunity would have been more personally beneficial than putative teaching. Whereas this study of chimpanzees technically satisfies Criterion 2 of animal teaching, it is important to qualify the results by understanding that the grade of cost was lower for parent chimpanzees than in other examples of teaching. As argued by Byrne and Rapaport (2011), these two studies certainly have contributed valuably to the field of animal teaching. However, I echo the concerns of Thornton and McAuliffe (2012) that researchers in this growing field must strive for high quality knowledge. That means clarifying—if not necessarily adhering to word for word—the nuances of the functional definition of teaching. In this essay I have aimed to clarify the purpose of cost in defining animal teaching. The fairy wren study has shown that we ought to functionally define cost as immediate and personal to the teacher, so to ensure that the putative teaching is cooperative. Furthermore, the chimpanzee study has highlighted the various grades of costs, and particularly that opportunity costs are less convincing than energy costs in deciding whether putative teachers are acting cooperatively rather than merely out of self-interest. I hope that future research can now benefit from a clearer understanding of the nuances of cost in animal teaching. The author thanks Professor Justin Harris and Dr. Mike Kendig for their support. REFERENCES Byrne RW, Rapaport LG. 2011. What are we learning from teaching? Anim Behav . 82: 1207– 1211. Google Scholar CrossRef Search ADS   Caro TM, Hauser MD. 1992. Is there teaching in nonhuman animals? Q Rev Biol . 67: 151– 174. Google Scholar CrossRef Search ADS PubMed  Colombelli-Négrel D, Hauber ME, Robertson J, Sulloway FJ, Hoi H, Griggio M, Kleindorfer S. 2012. Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr Biol . 22: 2155– 2160. Google Scholar CrossRef Search ADS PubMed  Kleindorfer S, Hoi H, Evans C, Mahr K, Robertson J, Hauber ME, Colombelli-Négrel D. 2014. The cost of teaching embryos in superb fairy-wrens. Behav Ecol . 25: 1131– 1135. Google Scholar CrossRef Search ADS   Musgrave S, Morgan D, Lonsdorf E, Mundry R, Sanz C. 2016. Tool transfers are a form of teaching among chimpanzees. Sci Rep . 6: 34783. Google Scholar CrossRef Search ADS PubMed  Raihani NJ, Ridley AR. 2008. Experimental evidence for teaching in wild pied babblers. Anim Behav . 75: 3– 11. Google Scholar CrossRef Search ADS   Thornton A, McAuliffe K. 2012. Teaching can teach us a lot. Anim Behav . 83: e6–e9. Thornton A, Raihani NJ. 2008. The evolution of teaching. Anim Behav . 75: 1823– 1836. Google Scholar CrossRef Search ADS   Thornton A, Raihani NJ. 2010. Identifying teaching in wild animals. Learn Behav . 38: 297– 309. Google Scholar CrossRef Search ADS PubMed  West SA, Griffin AS, Gardner A. 2007. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol . 20: 415– 432. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

Journal

Behavioral EcologyOxford University Press

Published: Jan 1, 2018

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