Comment on 'Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs'
- Department of Ecology, Evolution, and Organismal Biology, Brown University, United States
- Department of Evolutionary Biology, University of Vienna, Austria
- Vienna Zoo, Austria
Figures
Figure 1
Re-analysis of whether male little torrent frogs (Amolops torrentis) produce limb displays in the presence of parasites.
(A) Proportion of different limb displays observed passively in a population of males (n=69) either in the presence of parasites (blue bars) or in the absence of parasites (orange bars). Note that these data are weighted by the number of limb movements each male produced, which were highly skewed in the original dataset. In other words, in the first analysis by Zhao et al., some males produced >90 displays, whereas other males produced zero (Zhao et al., 2022). See Methods for details about how we weighted values. For all subsequent analyses (G-tests for goodness of fit), the proportion of toe trembling produced in the presence and absence of parasites was used as the null hypothesis, setting our expectation of how often displays should be produced by chance in the presence or absence of parasites (see Methods for justification). (B–F) Density plots of the boot strapped chi-squared (χ2) statistics from the G-test of goodness of fit analysis. On the y-axis is the density of chi-squared (χ2) statistics after 1,000 iterations, and on the x-axis is the chi-squared (χ2) value. Solid green lines denote mean chi-squared statistics associated with each distribution of values, whereas solid red lines represent the cut-off for statistical significance (P<0.05) with 1 degree of freedom. If the green line falls on the right side of the red line, then the result is statistically significant (i.e., male frogs appear to perform the given display in the presence of parasites more than we might expect by chance, as determined by the null model set through toe trembling). By contrast, if the green line falls on the left side of the red line, then the result is not significant (i.e., male frogs do not perform the given display in the presence of parasites more than we might expect by chance). We found that (B) toe trembling (TT) was (as expected) not statistically significant (χ2=0.084, P=0.772), nor was (C) hind foot lifting (HFL; χ2=0.487, P=0.485) or (D) arm wiping (AW; χ2=2.772, P=0.096). Importantly, these were the behaviors the females supposedly preferred, though see the main text for a discussion of the limitations associated with this assay. We found that (E) limb shaking behavior (LSA) was statistically significant (χ2=5.0314, P=0.025, denoted with asterisk), as was (F) wiping (W) (χ2=4.212, P=0.040, denoted with asterisk). These latter two behaviors (LSA and W) were not preferred by females in the behavioral assay. Note that when comparing A to both E and F (LSA and W, respectively), the proportions in A would suggest that the effect reported in F would be more robust, compared to the effect in E. However, there were several males that did not wipe (0 values), which may have broadened the Chi Squared curve and decreased the statistical power in the analysis.
Tables
Table 1
List of anuran species that perform limb displays or gestural signals.
For Dendrobatoidea, see Hödl and Amézquita, 2001. Note that in most cases the term courtship in the Behavioral Function column refers to instances in which females make choices about male mates, while males use gestural signals to simultaneously compete.
| Species* | Limb Signals | Sex | Behavioral Function | Evidence | Country of Origin | Ecology | Activity Pattern | Reference | |
|---|---|---|---|---|---|---|---|---|---|
| Brachychephalidae | Brachycephalus ephippium | arm waving | M | aggressive, defense | observation | Brazil | forest floor | diurnal | Pombal et al., 1994, Goutte et al., 2017 |
| B. pitanga | arm waving | M | aggressive, defense | observation | Brazil | forest floor, leaf litter | diurnal | Goutte et al., 2017 | |
| Bufonidae | Atelopus limosus | arm waving | M | context not determined | observation | Panama | stream | diurnal | Hödl and Amézquita, 2001 |
| A. varius | arm waving | M, F | aggressive, to defend sites | observation | Colombia, Costa Rica, Panama | stream | diurnal | Crump, 1988 | |
| A. zeteki | arm waving | M, F | M: agonistic, territorial vigilance, F: intersexual female-male, courtship | experimental/ mirror image | Panama | stream | diurnal | Lindquist and Hetherington, 1996, Lindquist and Hetherington, 1998 | |
| A. chiriquiensis | arm waving | M | call response, amplexus attempt | observation | Costa Rica, Panama | stream | diurnal | Lindquist and Hetherington, 1996, Lindquist and Hetherington, 1998 | |
| leg- kicking | M | during egg laying in amplexus | observation | Lindquist and Swihart, 1997 | |||||
| Leptodactylidae | Leptodactylus melanotus | foot twitching & back raise | M | aggressive | observation | Central America, Mexico | pond | Diurnal, nocturnal | Brattstrom, 1968, Gregory, 1983 |
| Crossodactylus gaudichaudii | arm waving | M | conspecific in the vicinity | observation | Brazil | stream | diurnal | Weygoldt and Potsch de Carvalho e Silva, 1992 | |
| leg stretch | M | aggressive | observation | Weygoldt and Potsch de Carvalho e Silva, 1992 | |||||
| leg lift | M | aggressive | observation | Weygoldt and Potsch de Carvalho e Silva, 1992 | |||||
| C. schmidtii | both legs kicking | M, J* | agonistic, *context not determined | observation | Brazil | stream | diurnal | Caldart et al., 2014 | |
| leg kicking | M | agonistic | observation | Caldart et al., 2014 | |||||
| toe flagging | M, F | agonistic | observation | Caldart et al., 2014 | |||||
| toe trembling | M | agonistic | observation | Caldart et al., 2014 | |||||
| limb lifting (arm & leg) | M, F, J | agonistic, M: courtship | observation | Caldart et al., 2014 | |||||
| Hylodes asper | foot flagging | M | agonistic, courtship | observation | Brazil | stream | diurnal | Haddad and Giaretta, 1999, Hartmann et al., 2005 | |
| toe movement, flagging | M | agonistic | observation | Haddad and Giaretta, 1999, Hartmann et al., 2005 | |||||
| leg stretching | M, F | M: agonistic; F: mating | observation, experimental (mirror) | Haddad and Giaretta, 1999, Hartmann et al., 2005 | |||||
| arm lifting | M | agonistic | observation | Haddad and Giaretta, 1999 | |||||
| kicking | M | aggressive | observation | Haddad and Giaretta, 1999 | |||||
| leg lifting | M | agonistic | observation | Hartmann et al., 2005 | |||||
| H. cardosoi | leg stretching (1 leg) | M | advertisement, courtship | observation | Brazil | stream | diurnal | Forti and Castanho, 2012 | |
| leg stretching (2 legs) | M | advertisement, courtship | observation | Forti and Castanho, 2012 | |||||
| limb lifting | M | advertisement, territorial | observation | Forti and Castanho, 2012 | |||||
| foot flagging | M, F | advertisement, courtship M: territorial | observation | Forti and Castanho, 2012 | |||||
| foot flagging +toe wave | M | advertisement, courtship, territorial | observation | Forti and Castanho, 2012 | |||||
| leg kicking | M | advertisement, courtship, territorial | observation | Forti and Castanho, 2012 | |||||
| H. dayctylocinus | foot flagging | M | agonistic, courtship | observation | Brazil | stream | diurnal | Narvaes and Rodrigues, 2005 | |
| toe wiggling | M | agonistic | observation | Narvaes and Rodrigues, 2005 | |||||
| leg stretching | M | agonistic | observation | Narvaes and Rodrigues, 2005 | |||||
| kicking | M | aggressive | observation | Narvaes and Rodrigues, 2005 | |||||
| arm lifting | M | context not determined | observation | Narvaes and Rodrigues, 2005 | |||||
| H. japi | toe trembling | M | agonistic, advertisement, courtship | observation | Brazil | stream | diurnal | de Sá et al., 2016 | |
| toe flagging | M | agonistic, advertisement, courtship | observation | de Sá et al., 2016 | |||||
| toes posture | M | agonistic, advertisement, courtship | observation | de Sá et al., 2016 | |||||
| foot shaking | M | agonistic, advertisement, courtship | observation | de Sá et al., 2016 | |||||
| leg stretching | M | agonistic | observation | de Sá et al., 2016 | |||||
| foot flagging | M | agonistic, advertisement, courtship | observation | de Sá et al., 2016 | |||||
| hand shaking | M | agonistic, advertisement, courtship | observation | de Sá et al., 2016 | |||||
| arm lifting | M,F | agonistic, courtship | observation | de Sá et al., 2016 | |||||
| arm waving | M,F | agonistic, courtship | observation | de Sá et al., 2016 | |||||
| H. meridionalis | toe flagging | M | agonistic | experimental | Brazil | stream | diurnal | de Sá et al., 2018, Furtado et al., 2019 | |
| toe trembling | M | agonistic | observation | de Sá et al., 2018, Furtado et al., 2019 | |||||
| toe posture | M | agonistic | observation, experimental | de Sá et al., 2018, Furtado et al., 2019 | |||||
| arm lifting | M, F | M-agonistic, F-reproductive | observation, experimental | de Sá et al., 2018, Furtado et al., 2019 | |||||
| arm waving | M, F | M-agonistic & reproductive, F-reproductive | observation, experimental | de Sá et al., 2018, Furtado et al., 2019 | |||||
| leg lifting | M, F | M-agonistic & reproductive, F-reproductive | observation, experimental | Furtado et al., 2019 | |||||
| foot flagging | M | agonistic | observation, experimental | Furtado et al., 2019 | |||||
| foot shaking | M | agonistic | observation | de Sá et al., 2018 | |||||
| both legs kicking | F | agonistic | observation | Furtado et al., 2019 | |||||
| H. nasus | toe wiggle | M | agonistic (threat signals) | observation, experimental | Brazil | stream | diurnal | Weber et al., 2004 | |
| arm waving | M | agonistic (threat signals) | observation, experimental | Weber et al., 2004 | |||||
| leg stretch | M | agonistic (threat signals) | observation, experimental | Weber et al., 2004 | |||||
| H. phyllodes | foot flagging | M | agonistic | observation, experimental | Brazil | stream | diurnal | Hartmann et al., 2005, Augusto-Alves and Toledo, 2021 | |
| leg stretching | M | agonistic, courtship | observation, experimental | Hartmann et al., 2005 | |||||
| arm lifting | M | agonistic, advertisement | observation, experimental | Hartmann et al., 2005, Augusto-Alves and Toledo, 2021 | |||||
| arm waving | M | context not determined | observation | Augusto-Alves and Toledo, 2021 | |||||
| leg lifting | M | agonistic, advertisement | observation, experimental | Hartmann et al., 2005, Augusto-Alves and Toledo, 2021 | |||||
| two limbs lifting | M | context not determined | observation | Augusto-Alves and Toledo, 2021 | |||||
| toe flagging | M | agonistic | observation, experimental | Hartmann et al., 2005, Augusto-Alves and Toledo, 2021 | |||||
| foot shaking | M | context not determined | observation | Augusto-Alves and Toledo, 2021 | |||||
| two-leg kicking | M | agonistic | observation | Augusto-Alves and Toledo, 2021 | |||||
| Myobatrachidae | Taudactylus eungellensis | leg stretching | M | context not determined | - | stream | diurnal | Hödl and Amézquita, 2001 | |
| foot flagging | M | context not determined | - | Hödl and Amézquita, 2001 | |||||
| Hylidae | Boana albomarginata | Limb lifting | M | agonistic | experimental (mirror) | Brazil | pond margins vegetation | nocturnal | Hartmann et al., 2005, Furtado and Nomura, 2014 |
| (Hypsiboas albomarginatus) | face wiping | M | agonistic | experimental (mirror) | Furtado and Nomura, 2014 | ||||
| (Hyla albormarginata) | toe trembling | M | agonistic | experimental (mirror) | Hartmann et al., 2005, Furtado and Nomura, 2014 | ||||
| leg kicking | M | agonistic | experimental (mirror) | Hartmann et al., 2005, Furtado and Nomura, 2014 | |||||
| B. raniceps | limb lifting | M | agonistic | experimental (mirror) | Brazil | ponds or wetlands | nocturnal | Furtado et al., 2017 | |
| (Hypsiboas raniceps) | toe/finger trembling | M | agonistic | experimental (mirror) | stream | nocturnal | Furtado et al., 2017 | ||
| Litoria cooloolensis | foot flagging | M | agonistic | observation | Australia | tree | nocturnal | Meyer et al., 2012 | |
| L. genimaculata | foot flagging | M | agonistic | observation | Australia | stream | nocturnal | Richards and James, 1992 | |
| L. iris | leg flicking | M | call response | observation | Papua New Guinea | stream | crepuscular | Meyer et al., 2012 | |
| L. nannotis | foot flagging | M | agonistic | observation | Australia | stream | nocturnal | Richards and James, 1992 | |
| arm waving | M | agonistic | observation | nocturnal | Richards and James, 1992 | ||||
| L. pearsoniana | hand waving | M | agonistic | observation | Australia | stream | nocturnal | Meyer et al., 2012 | |
| leg flicking | M | agonistic | observation | Meyer et al., 2012 | |||||
| L.rheocola | leg stretching | M | agonistic | observation | Australia | stream | nocturnal | Richards and James, 1992 | |
| arm waving | M | agonistic | observation | Richards and James, 1992 | |||||
| L. fallax | foot flagging | M | agonistic | observation | Australia | pond | nocturnal | Meyer et al., 2012 | |
| foot flickering | M | agonistic | observation | Meyer et al., 2012 | |||||
| kicking | M | aggressive | observation | Meyer et al., 2012 | |||||
| Lysapsus limellum | Limb lifting | M | agonistic | experimental (mirror) | Brazil | lentic water bodies | nocturnal | Furtado et al., 2017 | |
| Dendropsophus nanus | Limb lifting | M | agonistic | experimental (mirror) | Brazil | ponds | nocturnal | Furtado et al., 2017 | |
| Dendropsophus parviceps | foot flagging | M | agonistic | observation | Venezuela | streamside ponds | nocturnal | Amézquita and Hödl, 2004 | |
| Hyla parviceps | arm waving | M | agonistic | observation | Amézquita and Hödl, 2004 | ||||
| Hyla sp. (aff. ehrhardti) | body wiping (foot) | courtship | observation | Brazil | forest, bromeliads | nocturnal | Hartmann et al., 2005 | ||
| face wiping (arm) | M, F | courtship | observation | Hartmann et al., 2005 | |||||
| foot flagging | M | courtship (far from females) | observation | Hartmann et al., 2005 | |||||
| limb lifting (arm +leg) | M | courtship | observation | Hartmann et al., 2005 | |||||
| Phyllomedusa boliviana | foot flagging | M | aggressive | observation | Bolivia | pond | nocturnal | Jansen and Kohler, 2008 | |
| leg lifting | M | aggressive | observation | Jansen and Kohler, 2008 | |||||
| leg stretching | M | aggressive | observation | Jansen and Kohler, 2008 | |||||
| P. burmeisteri | leg stretching | M | agonistic | observation | Brazil | pond | nocturnal | Abrunhosa and Wogel, 2004 | |
| kicking | M | aggressive | observation | Abrunhosa and Wogel, 2004 | |||||
| P. sauvagii | foot flagging | M | territorial | observation | Argentina, Bolivia, Paraguay, Brazil | pond | nocturnal | Halloy and Espinoza, 2000 | |
| Scinax eurydice | leg kicking | M | 2 males far from each other | observation | Brazil | pond (rainy season) | nocturnal | Hartmann et al., 2005 | |
| limb lifting (arm +leg) | M | 2 males far from each other | observation | Hartmann et al., 2005 | |||||
| Centrolenidae | Vitreorana uranoscopa | limb lifting (arm +leg) | M | agonistic, spontaneous (no other individual present) | observation | Brazil | nocturnal | Hartmann et al., 2005 | |
| (Hyalinobatrachium uranoscopum) | |||||||||
| Ranidae | Pulchrana (Rana) baramica | toe waving | M | attract prey | observation | Singapore | forest | Grafe, 2008 | |
| Staurois latopalmatus | arm waving | M | agonistic | observation | Borneo | stream | diurnal | Preininger et al., 2009 | |
| foot flagging | M | agonistic | observation | Preininger et al., 2009 | |||||
| S. guttatus | foot flagging | M, F | agonistic | F-experimental, M-observation | stream | Grafe and Wanger, 2007, Preininger et al., 2016 | |||
| leg drumming | M | context not determined | observation | Grafe and Wanger, 2007 | |||||
| foot raising | M | courtship | observation | Grafe and Wanger, 2007 | |||||
| arm waving | M | agonistic | observation | Grafe and Wanger, 2007 | |||||
| S. parvus | foot flagging | M, J | agonistic | observation, experimental | Borneo | stream | diurnal | Grafe et al., 2012, Preininger et al., 2012, Preininger et al., 2013b | |
| foot lifting (tap) | M | agonistic | observation, experimental | Grafe et al., 2012, Preininger et al., 2013b | |||||
| Micrixalidae | Micrixalus candidus | foot lifting | M | agonistic | observation | India | stream | diurnal | Preininger and Fuxjager, pers. observation |
| foot stretching | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| M. elegans | foot lifting | M | agonistic | observation | India | stream | diurnal | Preininger and Fuxjager, pers. observation | |
| foot stretching | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| M. kottigeharensis | foot lifting | M | agonistic | observation | India | stream | diurnal | Preininger et al., 2013c, Anderson et al., 2021b, Anderson et al., 2021d | |
| foot stretching | M | agonistic | observation | Preininger et al., 2013b, Preininger et al., 2013c | |||||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| toe wiggling | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| kicking | M | aggressive | observation | Preininger et al., 2013c | |||||
| M. niluvasei | foot lifting | M | agonistic | observation | India | stream | Anderson et al., 2021d, Preininger and Fuxjager, pers. observation | ||
| foot stretching | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| kicking | M | aggressive | observation | Preininger and Fuxjager, pers. observation | |||||
| M. saxicola | foot lifting | M | agonistic | observation | India | stream | Anderson et al., 2021d, Preininger and Fuxjager, pers. observation | ||
| foot stretching | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| toe wiggling | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| kicking | M | aggressive | observation | Preininger and Fuxjager, pers. observation | |||||
| M. specca | foot lifting | M | agonistic | observation | India | stream | Preininger and Fuxjager, pers. observation | ||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| M. uttaraghati | foot lifting | M | agonistic | observation | India | stream | Preininger and Fuxjager, pers. observation | ||
| foot stretching | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| foot flagging | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| toe wiggling | M | agonistic | observation | Preininger and Fuxjager, pers. observation | |||||
| Rhacophoridae | Buergeria japonica | leg-stretches | M | agonistic male-male interaction | observation | Japan | aquatic and terrestrial | Anderson et al., 2021c | |
| B. otai | foot-flagging | M | agonistic male-male interaction | observation | Taiwan | stream | Yang, 2022 | ||
| Theloderma bambusicolum | foot-flagging | M | territorial behavior | observation | Vietnam | dense bushes | Orlov et al., 2012 |
-
*
Species names in parentheses represent former names used in original publication.
-
M=male; F=female; J=juvenile.
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Comment on 'Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs'
eLife 12:e89134.
https://doi.org/10.7554/eLife.89134
