Criteria for studies of dear enemy and nasty neighbor effects: a comment on Christensen and Radford

Criteria for studies of dear enemy and nasty neighbor effects: a comment on Christensen and Radford Christensen and Radford (2018) provide a masterful review of neighbor-stranger response differences (NSRD) in group-living species, one which is likely to spur further research on this topic. To that end, I here consider key criteria for determining whether territorial animals exhibit dear enemy (DE) or nasty neighbor (NN) effects, and list the studies of NSRD in group-living species that satisfy these criteria. The stimuli used to test for DE and NN effects can consist of strangers or neighbors themselves, or stimuli (e.g., songs, calls, scent marks) produced by strangers or neighbors. In either case, one needs to demonstrate that territory owners are capable of discriminating among the stimuli in question, even if they show comparable responses to stimuli from neighbors and strangers. For group-living territorial animals one way to do this is to include stimuli from same-group members in the experimental design. Differences in responses to stimuli from same-group members and from either neighbors or strangers indicate that a lack of either DE or NN effects is not a result of the subjects’ inability to discriminate among stimuli from different types of conspecifics (e.g., Botero et al. 2007). By definition, NN and DE are based on “defensive responses”, i.e., behavior patterns that under natural conditions reduce the probability that intruders will linger in the territory during a current visit, or will venture into the territory in the future. Of course, territory owners can express many different types of behavior when they encounter stimuli from intruders. For instance, animals often exhibit exploratory behavior when they encounter novel stimuli or when they encounter familiar stimuli in “unexpected” locations (e.g., Dix and Aggleton 1999; Dere et al. 2005). However, such behavior is assumed to function in information-acquisition, not defense. In addition, Christensen and Radford (2018) allude to situations in which some members of group-living species might express affiliative behavior toward particular categories of intruders (e.g., potential mates). Since territory owners can respond to stimuli from intruders using a wide range of behavior patterns, not all of which are defensive, simply demonstrating that territory residents respond differently to stimuli from neighbors and strangers is not sufficient to demonstrate DE or NN effects (see also below). Ideally, authors would specify the responses that they consider to be “defensive” before collecting any data on residents’ responses to stimuli from intruders. Responses to stimuli from neighbors and strangers should be scored within or at the boundary of space in which the resident group has been living for a period of time. This is because defensive behavior in territorial species is highly contingent on the extent to which the space in question is familiar to the “territory owner” (Stamps and Krishnan 1999). This condition is not satisfied in all experimental studies of NSRD in group-territorial animals. For instance, in 2 studies of social insects, aggressive interactions between residents, neighbors, and strangers were scored in neutral arenas that were novel to all of the subjects, including the “residents” (Dunn and Messier 1999; Sanada-Morimura et al. 2003). Since designations of DE and NN are currently based on statistically significant differences in defensive responses to neighbors and strangers, it is difficult to interpret situations in which the responses to neighbors and strangers are not significantly different (no detectable difference [NDD]). In future, it would be useful to present effect sizes, in addition to significance levels, in studies of NSRD. This would also facilitate future meta-analyses on this topic. Seven empirical studies of NSRD satisfied the criteria listed above (Table 1). There are 3 differences between the results indicated here and those listed for group-living species in Christensen and Radford (2018). First, Eurasian badgers, Meles meles, investigated the feces of stranger groups more than those of neighbor groups, results the authors interpreted as badgers investing time and effort to learn about the novel scents of strangers (Palphramand and White 2007). However, there were no differences in defensive behaviors that badgers expressed in response to the feces of strangers or neighbors, so I scored this study as NDD. Second, although Herbinger et al. (2009) reported that chimpanzees, Pan troglodytes, tended to produce aggressive (scream) vocalizations more often in response to the hoot-calls of neighbors than to those of strangers, this difference was not significant, so again, this study was scored as NDD. Finally, in the cooperatively breeding cichlid, Neolamprologus pulcher, “simulated intrusions of non-neighboring individuals led to higher total levels of defense behavior by residents than intrusions from neighbors” (Bruintjes et al. 2016), so I placed this species in the DE category. Table 1 Studies of NSRD in group-living animals which satisfy criteria for inclusion Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Scores are based on differences in defensive behavior exhibited in response to stimuli from neighbors and strangers. View Large Table 1 Studies of NSRD in group-living animals which satisfy criteria for inclusion Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Scores are based on differences in defensive behavior exhibited in response to stimuli from neighbors and strangers. View Large This quick survey indicates that there is plenty of scope for additional studies of NSRD in group-living territorial animals (Table 1). REFERENCES Botero CA, Riveros JM, Vehrencamp SL. 2007. Relative threat and recognition ability in the responses of tropical mockingbirds to song playback. Anim Behav . 73: 661– 669. Google Scholar CrossRef Search ADS PubMed  Bruintjes R, Lynton-Jenkins J, Jones JW, Radford AN. 2016. Out-group threat promotes within-group affiliation in a cooperative fish. Am Nat . 187: 274– 282. Google Scholar CrossRef Search ADS PubMed  Christensen C, Radford AN. 2018. Dear enemies or nasty neighbours? Causes and consequences of variation in the responses of group-living species to territorial intrusions. Behav Ecol . doi.org/10.1093/beheco/ary010. Dere E, Huston JP, De Souza Silva MA. 2005. Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice. Neurobiol Learn Mem . 84: 214– 221. Google Scholar CrossRef Search ADS PubMed  Dix SL, Aggleton JP. 1999. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res . 99: 191– 200. Google Scholar CrossRef Search ADS PubMed  Dunn R, Messier S. 1999. Evidence for the opposite of the dear enemy phenomenon in termites. J Insect Behav . 12: 461– 464. Google Scholar CrossRef Search ADS   Herbinger I, Papworth S, Boesch C, Zuberbuhler K. 2009. Vocal, gestural and locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Animal Behav . 78: 1389– 1396. Google Scholar CrossRef Search ADS   Muller CA, Manser MB. 2007. ‘Nasty neighbours’ rather than ‘dear enemies’ in a social carnivore. Proc Biol Sci . 274: 959– 965. Google Scholar CrossRef Search ADS PubMed  Newey PS, Robson SK, Crozier RH. 2010. Weaver ants Oecophylla smaragdina encounter nasty neighbors rather than dear enemies. Ecology . 91: 2366– 2372. Google Scholar CrossRef Search ADS PubMed  Palphramand KL, White PCL. 2007. Badgers, Meles meles, discriminate between neighbour, alien and self scent. Animal Behav . 74: 429– 436. Google Scholar CrossRef Search ADS   Radford AN. 2005. Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green woodhoopoe. Animal Behav . 70: 1227– 1234. Google Scholar CrossRef Search ADS   Sanada-Morimura S, Minai M, Yokoyama M, Hirota T, Satoh T, Obara Y. 2003. Encounter-induced hostility to neighbors in the ant Pristomyrmex pungens. Behav Ecol . 14: 713– 718. Google Scholar CrossRef Search ADS   Stamps JA, Krishnan VV. 1999. A learning-based model of territory establishment. Q Rev Biol . 74: 291– 318. Google Scholar CrossRef Search ADS   © The Author(s) 2018. 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 This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Criteria for studies of dear enemy and nasty neighbor effects: a comment on Christensen and Radford

Behavioral Ecology , Volume Advance Article – Apr 6, 2018

Loading next page...
 
/lp/ou_press/criteria-for-studies-of-dear-enemy-and-nasty-neighbor-effects-a-Gg0pRq3aE0
Publisher
Oxford University Press
Copyright
© The Author(s) 2018. 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
ISSN
1045-2249
eISSN
1465-7279
D.O.I.
10.1093/beheco/ary033
Publisher site
See Article on Publisher Site

Abstract

Christensen and Radford (2018) provide a masterful review of neighbor-stranger response differences (NSRD) in group-living species, one which is likely to spur further research on this topic. To that end, I here consider key criteria for determining whether territorial animals exhibit dear enemy (DE) or nasty neighbor (NN) effects, and list the studies of NSRD in group-living species that satisfy these criteria. The stimuli used to test for DE and NN effects can consist of strangers or neighbors themselves, or stimuli (e.g., songs, calls, scent marks) produced by strangers or neighbors. In either case, one needs to demonstrate that territory owners are capable of discriminating among the stimuli in question, even if they show comparable responses to stimuli from neighbors and strangers. For group-living territorial animals one way to do this is to include stimuli from same-group members in the experimental design. Differences in responses to stimuli from same-group members and from either neighbors or strangers indicate that a lack of either DE or NN effects is not a result of the subjects’ inability to discriminate among stimuli from different types of conspecifics (e.g., Botero et al. 2007). By definition, NN and DE are based on “defensive responses”, i.e., behavior patterns that under natural conditions reduce the probability that intruders will linger in the territory during a current visit, or will venture into the territory in the future. Of course, territory owners can express many different types of behavior when they encounter stimuli from intruders. For instance, animals often exhibit exploratory behavior when they encounter novel stimuli or when they encounter familiar stimuli in “unexpected” locations (e.g., Dix and Aggleton 1999; Dere et al. 2005). However, such behavior is assumed to function in information-acquisition, not defense. In addition, Christensen and Radford (2018) allude to situations in which some members of group-living species might express affiliative behavior toward particular categories of intruders (e.g., potential mates). Since territory owners can respond to stimuli from intruders using a wide range of behavior patterns, not all of which are defensive, simply demonstrating that territory residents respond differently to stimuli from neighbors and strangers is not sufficient to demonstrate DE or NN effects (see also below). Ideally, authors would specify the responses that they consider to be “defensive” before collecting any data on residents’ responses to stimuli from intruders. Responses to stimuli from neighbors and strangers should be scored within or at the boundary of space in which the resident group has been living for a period of time. This is because defensive behavior in territorial species is highly contingent on the extent to which the space in question is familiar to the “territory owner” (Stamps and Krishnan 1999). This condition is not satisfied in all experimental studies of NSRD in group-territorial animals. For instance, in 2 studies of social insects, aggressive interactions between residents, neighbors, and strangers were scored in neutral arenas that were novel to all of the subjects, including the “residents” (Dunn and Messier 1999; Sanada-Morimura et al. 2003). Since designations of DE and NN are currently based on statistically significant differences in defensive responses to neighbors and strangers, it is difficult to interpret situations in which the responses to neighbors and strangers are not significantly different (no detectable difference [NDD]). In future, it would be useful to present effect sizes, in addition to significance levels, in studies of NSRD. This would also facilitate future meta-analyses on this topic. Seven empirical studies of NSRD satisfied the criteria listed above (Table 1). There are 3 differences between the results indicated here and those listed for group-living species in Christensen and Radford (2018). First, Eurasian badgers, Meles meles, investigated the feces of stranger groups more than those of neighbor groups, results the authors interpreted as badgers investing time and effort to learn about the novel scents of strangers (Palphramand and White 2007). However, there were no differences in defensive behaviors that badgers expressed in response to the feces of strangers or neighbors, so I scored this study as NDD. Second, although Herbinger et al. (2009) reported that chimpanzees, Pan troglodytes, tended to produce aggressive (scream) vocalizations more often in response to the hoot-calls of neighbors than to those of strangers, this difference was not significant, so again, this study was scored as NDD. Finally, in the cooperatively breeding cichlid, Neolamprologus pulcher, “simulated intrusions of non-neighboring individuals led to higher total levels of defense behavior by residents than intrusions from neighbors” (Bruintjes et al. 2016), so I placed this species in the DE category. Table 1 Studies of NSRD in group-living animals which satisfy criteria for inclusion Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Scores are based on differences in defensive behavior exhibited in response to stimuli from neighbors and strangers. View Large Table 1 Studies of NSRD in group-living animals which satisfy criteria for inclusion Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Species  Stimulus  Defensive Response  Reference  Green woodhoopoes  Call playbacks  DE  Radford 2005  Mockingbirds  Song playbacks  NDD  Botero et al. 2007  Banded mongoose  Scent marks  NN  Muller and Manser 2007  Chimpanzees  Call playbacks  NDD  Herbinger et al. 2009  Badgers  Faeces  NDD  Palphramand and White 2007  Weaver ants  Neighbors and Strangers  NN  Newey et al. 2010  Cichlid (N. pulcher)  Neighbors and Strangers  DE  Bruintjes et al. 2016  Scores are based on differences in defensive behavior exhibited in response to stimuli from neighbors and strangers. View Large This quick survey indicates that there is plenty of scope for additional studies of NSRD in group-living territorial animals (Table 1). REFERENCES Botero CA, Riveros JM, Vehrencamp SL. 2007. Relative threat and recognition ability in the responses of tropical mockingbirds to song playback. Anim Behav . 73: 661– 669. Google Scholar CrossRef Search ADS PubMed  Bruintjes R, Lynton-Jenkins J, Jones JW, Radford AN. 2016. Out-group threat promotes within-group affiliation in a cooperative fish. Am Nat . 187: 274– 282. Google Scholar CrossRef Search ADS PubMed  Christensen C, Radford AN. 2018. Dear enemies or nasty neighbours? Causes and consequences of variation in the responses of group-living species to territorial intrusions. Behav Ecol . doi.org/10.1093/beheco/ary010. Dere E, Huston JP, De Souza Silva MA. 2005. Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice. Neurobiol Learn Mem . 84: 214– 221. Google Scholar CrossRef Search ADS PubMed  Dix SL, Aggleton JP. 1999. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res . 99: 191– 200. Google Scholar CrossRef Search ADS PubMed  Dunn R, Messier S. 1999. Evidence for the opposite of the dear enemy phenomenon in termites. J Insect Behav . 12: 461– 464. Google Scholar CrossRef Search ADS   Herbinger I, Papworth S, Boesch C, Zuberbuhler K. 2009. Vocal, gestural and locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Animal Behav . 78: 1389– 1396. Google Scholar CrossRef Search ADS   Muller CA, Manser MB. 2007. ‘Nasty neighbours’ rather than ‘dear enemies’ in a social carnivore. Proc Biol Sci . 274: 959– 965. Google Scholar CrossRef Search ADS PubMed  Newey PS, Robson SK, Crozier RH. 2010. Weaver ants Oecophylla smaragdina encounter nasty neighbors rather than dear enemies. Ecology . 91: 2366– 2372. Google Scholar CrossRef Search ADS PubMed  Palphramand KL, White PCL. 2007. Badgers, Meles meles, discriminate between neighbour, alien and self scent. Animal Behav . 74: 429– 436. Google Scholar CrossRef Search ADS   Radford AN. 2005. Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green woodhoopoe. Animal Behav . 70: 1227– 1234. Google Scholar CrossRef Search ADS   Sanada-Morimura S, Minai M, Yokoyama M, Hirota T, Satoh T, Obara Y. 2003. Encounter-induced hostility to neighbors in the ant Pristomyrmex pungens. Behav Ecol . 14: 713– 718. Google Scholar CrossRef Search ADS   Stamps JA, Krishnan VV. 1999. A learning-based model of territory establishment. Q Rev Biol . 74: 291– 318. Google Scholar CrossRef Search ADS   © The Author(s) 2018. 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 This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

Behavioral EcologyOxford University Press

Published: Apr 6, 2018

There are no references for this article.

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