Teaching behavior is responsive and costly in fairy-wrens though the time course needs to be defined

Teaching behavior is responsive and costly in fairy-wrens though the time course needs to be defined By definition, teaching is both cooperative and costly and so we appreciate Cordony’s (2017) commentary in this spirit. We also agree that the cost of teaching in the superb fairy-wren (Malurus cyaneus) system can and should be more fully explored. Kleindorfer, Hoi, et al. (2014) quantified a cost of incubation calling (Colombelli-Négrel et al. 2012) to fairy-wren mothers through the detection of higher egg predation at nests with more incubation calls. The commentary raises 2 main concerns: that 1) Kleindorfer, Hoi, et al. (2014) misinterpreted the operational definition of cost in animal teaching by Caro and Hauser (1992) and its operational interpretation by Thornton and Raihani (2010), because 2) nest predation is neither an immediate nor a personal cost to the mother. Regarding (1), as Cordony (2017) points out, criterion 2 of the Caro and Hauser (1992, p. 153) operational definition of animal teaching requires that the teacher experiences “some cost or at least without obtaining an immediate benefit.” Kleindorfer, Hoi, et al. (2014) did not misinterpret this component of the operational definition by not showing an immediate cost to the calling female fairy-wrens as suggested by Cordony (2017), because there is no such obligatory requirement in the Caro and Hauser definition. In fact, Cordony (2017) considers the fairy-wren example as a strong example for teaching, because there is no clear, immediate benefit to the female in this system. Furthermore, Cordony (2017) also disagrees with criterion 2 derived from the Caro and Hauser operational definition and suggests that “the cost of teaching must be personal and immediate.” This is a suggested modification by Thornton and Raihani (2010) of the 1992 definition, and advocated by Cordony, but it is not part of that original work, which was the only definitional study used and referenced by us in the 2014a study. Regarding (2), we originally showed that teaching in the fairy-wren system “carries a potentially high cost as the risk of predation was much higher when there were many incubation calls at both natural and artificial nests” (Kleindorfer, Hoi, et al. 2014, p. 1134). Cordony (2017) argues that the “personal costs to the parent remained untested” and instead that it is only a cost paid by the pupils. We disagree with this claim, since the female is 50% related to her entire clutch (in the absence of conspecific parasitism) and as such, pays a severe cost (e.g., lower fitness, higher energetic cost of renesting) for losing her full clutch and current breeding attempt due to vocalization-related predation. Whether this predation cost is delayed temporally (i.e., not immediate following incubation calling) and whether the same predation also represents a cost to the pupil (the embryo inside the egg) does not contradict the Caro and Hauser (1992) definition of teaching. There is evidence across systems that songbirds rapidly and adaptively adjust their vocalization behavior to the perceived threat of predation and brood parasitism (e.g., Platzen & Magrath 2004; Kleindorfer, Evans, et al. 2014), suggesting the capacity to associate different types of vocalization behavior with different levels of predation risk. Although not quantified by us in the study, it is likely that nest predation on eggs also carries a further personal cost to the calling mother who is confined in an enclosed nest during incubation and becomes more susceptible to predation herself. We showed higher nest predation (and hence nest visitation by predators) when a nest emanates many vocalizations, which has been found across studies (e.g., Platzen & Magrath 2004; Kleindorfer et al. 2016). Our previous research using video recordings at nests documented nest visitation by Grey Currawong (Strepera versicolor) and Sparrowhawk (Accipiter nisus) (Colombelli-Négrel et al. 2009), both known predators of adult fairy-wrens. Therefore, attending adults are exposed to the risk of predator detection. Second, we agree with the commentary, but again not quantified in our study, that vocalization behavior carries both an immediate energetic cost for production of sound and an opportunity cost for less time to forage and self-maintain. As discussed above, across songbird systems, there is evidence that vocalization behavior at the nest increases the personal risk of predation for the attending adult, lowers individual fitness given increased offspring mortality, increases investment cost per nesting attempt if predation leads to a replacement clutch, and increases metabolic costs during vocalization events Thomas 2002; Ward et al. 2003; Hasselquist and Bensch 2008. In conclusion, we support the tenor of the commentary in general and encourage future study into the personal cost of teaching and other aspects of parental care activity at the nest of fairy-wrens and other taxa. We maintain the view that, in support of our chosen operational definition of teaching, we have shown that the superb fairy-wren system involves a fitness cost to the teacher through increased offspring predation. REFERENCES 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, Robertson J, Kleindorfer S. 2009. A new audio-visual technique for effectively monitoring nest predation and the behaviour of nesting birds. Emu . 109: 83– 88. Google Scholar CrossRef Search ADS   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  Cordony M. 2017. Misinterpreting ‘cost’ in the classification of animal teaching. Behav Ecol . 29:e1–e2. Hasselquist D, Bensch S. 2008. Daily energy expenditure of singing great reed warblers Acrocephalus arundinaceus. J Avian Biol. 39: 384–388. 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   Kleindorfer S, Evans C, Colombelli-Négrel D. 2014. Females that experience threat are better teachers. Biol Lett . 10: 20140046. Google Scholar CrossRef Search ADS PubMed  Kleindorfer S, Evans C, Mahr K. 2016. Female in-nest chatter song increases predation. Biol Lett . 12: 20150513. Google Scholar CrossRef Search ADS PubMed  Platzen D, Magrath RD. 2004. Parental alarm calls suppress nestling vocalization. Proc Biol Sci . 271: 1271. Google Scholar CrossRef Search ADS PubMed  Thomas RJ. 2002. The costs of singing in nightingales. Anim Behav. 63: 959–966. Thornton A, Raihani NJ. 2010. Identifying teaching in wild animals. Learn Behav . 38: 297– 309. Google Scholar CrossRef Search ADS PubMed  Ward S, Speakman JR, Slater PJ. 2003. The energy cost of song in the canary, Serinus canaria. Anim Behav. 66: 893–902. © 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

Teaching behavior is responsive and costly in fairy-wrens though the time course needs to be defined

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Oxford University Press
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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

By definition, teaching is both cooperative and costly and so we appreciate Cordony’s (2017) commentary in this spirit. We also agree that the cost of teaching in the superb fairy-wren (Malurus cyaneus) system can and should be more fully explored. Kleindorfer, Hoi, et al. (2014) quantified a cost of incubation calling (Colombelli-Négrel et al. 2012) to fairy-wren mothers through the detection of higher egg predation at nests with more incubation calls. The commentary raises 2 main concerns: that 1) Kleindorfer, Hoi, et al. (2014) misinterpreted the operational definition of cost in animal teaching by Caro and Hauser (1992) and its operational interpretation by Thornton and Raihani (2010), because 2) nest predation is neither an immediate nor a personal cost to the mother. Regarding (1), as Cordony (2017) points out, criterion 2 of the Caro and Hauser (1992, p. 153) operational definition of animal teaching requires that the teacher experiences “some cost or at least without obtaining an immediate benefit.” Kleindorfer, Hoi, et al. (2014) did not misinterpret this component of the operational definition by not showing an immediate cost to the calling female fairy-wrens as suggested by Cordony (2017), because there is no such obligatory requirement in the Caro and Hauser definition. In fact, Cordony (2017) considers the fairy-wren example as a strong example for teaching, because there is no clear, immediate benefit to the female in this system. Furthermore, Cordony (2017) also disagrees with criterion 2 derived from the Caro and Hauser operational definition and suggests that “the cost of teaching must be personal and immediate.” This is a suggested modification by Thornton and Raihani (2010) of the 1992 definition, and advocated by Cordony, but it is not part of that original work, which was the only definitional study used and referenced by us in the 2014a study. Regarding (2), we originally showed that teaching in the fairy-wren system “carries a potentially high cost as the risk of predation was much higher when there were many incubation calls at both natural and artificial nests” (Kleindorfer, Hoi, et al. 2014, p. 1134). Cordony (2017) argues that the “personal costs to the parent remained untested” and instead that it is only a cost paid by the pupils. We disagree with this claim, since the female is 50% related to her entire clutch (in the absence of conspecific parasitism) and as such, pays a severe cost (e.g., lower fitness, higher energetic cost of renesting) for losing her full clutch and current breeding attempt due to vocalization-related predation. Whether this predation cost is delayed temporally (i.e., not immediate following incubation calling) and whether the same predation also represents a cost to the pupil (the embryo inside the egg) does not contradict the Caro and Hauser (1992) definition of teaching. There is evidence across systems that songbirds rapidly and adaptively adjust their vocalization behavior to the perceived threat of predation and brood parasitism (e.g., Platzen & Magrath 2004; Kleindorfer, Evans, et al. 2014), suggesting the capacity to associate different types of vocalization behavior with different levels of predation risk. Although not quantified by us in the study, it is likely that nest predation on eggs also carries a further personal cost to the calling mother who is confined in an enclosed nest during incubation and becomes more susceptible to predation herself. We showed higher nest predation (and hence nest visitation by predators) when a nest emanates many vocalizations, which has been found across studies (e.g., Platzen & Magrath 2004; Kleindorfer et al. 2016). Our previous research using video recordings at nests documented nest visitation by Grey Currawong (Strepera versicolor) and Sparrowhawk (Accipiter nisus) (Colombelli-Négrel et al. 2009), both known predators of adult fairy-wrens. Therefore, attending adults are exposed to the risk of predator detection. Second, we agree with the commentary, but again not quantified in our study, that vocalization behavior carries both an immediate energetic cost for production of sound and an opportunity cost for less time to forage and self-maintain. As discussed above, across songbird systems, there is evidence that vocalization behavior at the nest increases the personal risk of predation for the attending adult, lowers individual fitness given increased offspring mortality, increases investment cost per nesting attempt if predation leads to a replacement clutch, and increases metabolic costs during vocalization events Thomas 2002; Ward et al. 2003; Hasselquist and Bensch 2008. In conclusion, we support the tenor of the commentary in general and encourage future study into the personal cost of teaching and other aspects of parental care activity at the nest of fairy-wrens and other taxa. We maintain the view that, in support of our chosen operational definition of teaching, we have shown that the superb fairy-wren system involves a fitness cost to the teacher through increased offspring predation. REFERENCES 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, Robertson J, Kleindorfer S. 2009. A new audio-visual technique for effectively monitoring nest predation and the behaviour of nesting birds. Emu . 109: 83– 88. Google Scholar CrossRef Search ADS   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  Cordony M. 2017. Misinterpreting ‘cost’ in the classification of animal teaching. Behav Ecol . 29:e1–e2. Hasselquist D, Bensch S. 2008. Daily energy expenditure of singing great reed warblers Acrocephalus arundinaceus. J Avian Biol. 39: 384–388. 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   Kleindorfer S, Evans C, Colombelli-Négrel D. 2014. Females that experience threat are better teachers. Biol Lett . 10: 20140046. Google Scholar CrossRef Search ADS PubMed  Kleindorfer S, Evans C, Mahr K. 2016. Female in-nest chatter song increases predation. Biol Lett . 12: 20150513. Google Scholar CrossRef Search ADS PubMed  Platzen D, Magrath RD. 2004. Parental alarm calls suppress nestling vocalization. Proc Biol Sci . 271: 1271. Google Scholar CrossRef Search ADS PubMed  Thomas RJ. 2002. The costs of singing in nightingales. Anim Behav. 63: 959–966. Thornton A, Raihani NJ. 2010. Identifying teaching in wild animals. Learn Behav . 38: 297– 309. Google Scholar CrossRef Search ADS PubMed  Ward S, Speakman JR, Slater PJ. 2003. The energy cost of song in the canary, Serinus canaria. Anim Behav. 66: 893–902. © 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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