Comparing morphological traits of legs of understory birds inhabiting forest areas with closed canopies and forest gaps
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Abstract. Siri S, Ponpituk Y, Safoowong M, Nuipakdee W, Marod D, Duangkae P. 2020. Comparing morphological traits of legs of understory birds inhabiting forest areas with closed canopies and forest gaps. Biodiversitas 21: 1041-1048. Bird species exhibit different adaptations depending on their habitats. The morphological traits of each species represent adaptations that are impacted by environmental changes. We conducted a 3-year study from 2015 to 2017 to compare the leg morphology of understory birds that occur under closed canopies and in forest gaps in a hill evergreen forest in northern Thailand, with gaps in the natural forest representing forest disturbances. We captured 64 bird species over the study period and measured 11 leg morphological features for each individual. Ground-foraging birds were generally long-legged and climbing birds generally short-legged. Understory species living in dense forest areas were significantly associated with long claws, toes, and tibiae, whereas species occurring in gaps and open areas tended to have shorter leg structures. Results from classification tree analysis revealed that digit claw length is the most important trait for predicting which habitat a species is most likely to occupy. Our findings suggest that understory birds with long leg structures that live under closed canopies are most vulnerable to forest disturbances or the conversion of forests to large-scale open areas.
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References
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Barbosa A, Moreno E. 1999. Hindlimb morphology and locomotion performance in waders: an evolutionary approach. Biol J Linn Soc. 67: 313–330.
Birn-Jeffery AV, Miller CE, Naish D et al. 2012. Pedal claw curvature in birds, compensating for mass-specific and phylogenetic control. PLoS One. doi:10.1371/journal.pone.0050555
Dilger WC. 1956. Adaptive modifications and ecological isolating mechanism in the thrush genera Catharus and Hylocichla. Wilson Bull. 68: 171–199.
De souza O, Schoereder JH, Brown V et al. 2001. A theoretical overview of the processes determining species richness in forest fragment. In: Bierregaard RO Jr, Gascon C, Lovejoy TE, Mesquita R (eds). Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest. Yale Univ. Press, New Haven, London.
Dehling DM, Jordano P, Schaefer HM et al. 2016. Morphology predicts species’ functional roles and their degree of specialization in plant-frugivore interactions. PROY SOC B BIOL SCI. doi.org/10.1098/rspb.2015.2444
Grant PR. 1965. The adaptive significance of some size trends in Island birds. Evolution 19: 355–367.
Grant PR. 1971. Variation in the tarsus length of birds in island and mainland regions. Evolution 25: 599–614.
Grant PR. 1986. Bill size, body size, and the ecological adaptation of bird species to competitive situations on island. Syst. Zool. 17: 319–333.
Greenberg R. 1989. Neophobia, aversion to open space, and ecological plasticity in song and swamp sparrows. Can. J. Zool. 67: 1194–1199.
Garnier E, Cortez J, Billes G et al. 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecological Society of America. 85: 2630–2637.
Gilroy J, Uribe CAM, Haugaasen T et al. 2014. Effect of scale on trait predictor of species responses to agriculture. Conserv Biol. 29: 463–472.
Glomvinya S, Tantasirin C, Tongdeenok P et al. 2016. Change in rainfall characteristics at Huai Kog-Ma watershed, Chiang Mai Province. Thai J For. 35: 66–77.
James FC. 1982. The ecological morphology of birds: a review. Animal. Zoologici Fennici. 19: 265–275.
Karr JR, Freemark KE. 1983. Habitat selection and environmental gradients: dynamics in the “stable” tropics. Ecological Society of America. 64: 1481–1494.
Kováts D, Harnos A. 2005. Morphological classification of conspecific birds from closely situated breeding areas – A case study of the Common Nightingale. Ornis Hung. 23(2): 20–30.
McNamara JM, Houston AI. 1990. The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheor. 38(1): 37–61.
MacLeod MG, Valentine J, Cowan A, Wade A, McNeil L, Bernard K. 2008. Metabolisable energy yield from a range of varieties in broilers, cockerels and turkeys. Br. Poult. Sci. 49: 368–377.
Marod D, Kutintara U. 2009. Forest Ecology. Faculty of Forestry, Kasetsart University. Bangkok.
Marod D, Sungkaew S, Duengkae P, et al. 2014. Plant diversity of lower montane evergreen forest at Huai Kogma watershed area, Doi Suthep-Pui National Park, Chiang Mai province. In: Marod D, Thapyai C (eds) Thai forest ecological research network, T-FERN ecological knowledge for sustainable management. Naresuan University, 22-23 January 2015. [Thailand]
Nussey DH, Wilson AJ, Brommer JE. 2007. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20: 831–844.
Newbold T, Scharlemann JPW, Butchart SHH et al. 2012. Ecological traits affect the response of tropical forest bird species to land-use intensity. Proc. R. Soc. Lond. doi: 10.1098/rspb.2012.2131
Osterhaus MB. 1962. Modifications in the leg structure of some North American Warblers. Am Midl Nat. 68: 474–486.
Payne RB, Risley CJ. 1976. Systematics and evolutionary relationships among the Heron (Ardeidae). Museum of Zoology, University of Michigan, Michigan.
Pfenning DW, Wund MA, Snell-Rood EC et al. 2010. Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol. 25: 459–467.
Powell LL, Stouffer PC, Johnson ET. 2013. Recovery of understory bird movement across the interface of primary and secondary Amazon rainforest. Auk. 130: 459–468.
Powell T, Norbert J, Cordeiro J, Stratford A. 2015. Ecology and conservation of avian insectivores of the rainforest understory: a pantropical perspective. Biol. Conserv. 188: 1–10.
Phillips HRP, Newbold T, Purvis A. 2017. Land-use effect on local biodiversity in tropical forests vary between continents. Biodivers Conserv. 26: 2251–2270.
Pratumtong D, Gale GA, Duengkae P, Pongpattananurak N, Chimchome V. 2018. The influence of environmental variables on bird communities in tropical seasonal forests, western Thailand. JWT. 25: 49–65.
Richardson F. 1942. Adaptive modification for tree-trunk foraging in birds. Univ. Calif. publ. zool. 46: 317–368.
Raffaelli DG, Frid CLJ. 2010. Ecosystem Ecology: A New Synthesis. Cambridge University Press, Cambridge.
Round PD, Andrew JP, Wangworn S, George AG. 2011. The avifauna of the Mo Singto forest dynamics plot, Khao Yai National Park, Thailand. Nat. Hist. Bull. Siam. Soc. 57: 57-80.
R Core Team. 2014. R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria.
Rolo V, Olivier PI, van Aarde R. 2017. Tree and bird functional groups as indicators of recovery at generating subtropical coastal dune forest. Restor. Ecol. 25: 788–797.
Storer RW. 1960. Adaptive radiation in birds. In: Marshall A.J. ed. Biology and comparative physiology of birds, Vol 1. Academic Press, New York.
Schulenberg TS. 1983. Foraging behavior, eco-morphology, and systematic of some antshrikes (Formicariidae: Thamnomanse). Wilson bull. 95: 505–521.
Stratford JA, Stouffer PC. 1999. Local extinctions of terrestrial insectivorous birds in a fragmented landscape near Manaus, Brazil. Conserv Biol. 13: 1416–1423.
Schliemann SA, Bockheim JG. 2011. Methods for studying treefall gaps: a review. For. Ecol. Manag. 261: 1143–1151.
Siri S, Duengkae P, Marod D. 2013. Species diversity and abundance of birds in hill evergreen forest permanent plot at Huai Kok Ma, Chiang Mai province. JWT. 20: 97–112.
Sreekar R, Srinivasan U, Mammides C et al. 2015. The effect of land-use on the diversity and mass-abundance relationships of understory avian insectivores in Sri Lanka and southern India. Sci. Rep. 5: 11569 DOI: 10.1038/srep11569
Stratford JA, Stouffer PC. 2015. Forest fragmentation alters microhabitat availability for neotropical terrestrial insectivore birds. Biol. Conserv. 188: 109–115.
Shao S, Quan Q, Cai S, Qu Y, Lei F. 2016. Evolution of body morphology and beak shape revealed by a morphometric analysis of 14 Paridae species. Front Zool. 13: 30. doi.org/10.1186/s12983-016-0162-0
Shatkovska OV, Ghazali M. 2017. Relationship between developmental modes, flight styles and wing morphology in birds. European Journal of Zoological Research. 84: 390–401.
Siri S, Ponpituk Y, Safoowong M, Marod D, Duengkae P. 2019. The natural forest gaps maintenance diversity of understory birds in Mae Sa-Kog Ma Biosphere Reserve, northern Thailand. Biodiversitas 20: 181–189.
Srinivasan U. 2019. Morphological and behavioral correlates of long-term bird survival in selectively logged forest. Front Ecol Evol. 7:17. doi: 10.3389/fevo.2019.00017
Thiollay JM. 1992. Influence of selective logging on bird species diversity in a Guianan rain forest. Conserv Biol. 6: 47–63.
Thuiller W, Pironon S, Psomas A et al. 2014. The European functional tree of bird life in the face of global change. Nat. Commun. 5: 3118. DOI: 10.1038/ncomms4118
Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E. 2007. Let the concept of trait be functional!. Oikos 116: 882–892.
Vu LV. 2009. Diversity and similarity of butterfly communities in five different habitat types at Tam Dao National Park, Vietnam. J. Zool. 277: 15–22.
Winkler H, Bock W. 1976. Analyse der Kräfteverhältnisse bei Klettervögeln. J. Ornithol. 117: 397–418.
Whelan CJ. 2001. Foliage structure influences foraging of insectivorous forest bird: an experimental study. Ecological Society of America. 82: 219–231.
Walther BA. 2002. Vertical stratification and use of vegetation and light habitat by Neotropical forest birds. J. Ornithol. 143: 64–81.
Wunderle JM, Willig RMR, Henriques LMP. 2005. Avian distribution in treefall gaps and understorey of terra firme forest in the lowland Amazon. Ibis. 147: 109–129.
Werema C. 2015. Seasonal variation in understory bird species diversity and abundance in the Uluguru Nature Reserve, Tanzania. Afr. J. Ecol. 54: 299–307.
Xing L, Jingmai K, Connor Q et al. 2019. A new enantiornithine bird with unusual pedal proportions found in amber. Curr Biol. 29(14): 2396–2401.
Zeffer A, Johansson LC, Marmebro A. 2003. Functional correlation between habitat use and leg morphology in birds (Aves). Biol J Linn Soc. 79: 461–481.
Baldwin SP, Oberholser HC, Worley LG. 1931. Measurements of birds. Cleveland Museum of Natural, Ohio.
Bennett MB. 1996. Allometry of the leg muscles of birds. J. Zool., Lond. 238: 435–443.
Bibby C, Jones M, Marsden S. 1998. Expedition field techniques: bird surveys. Royal Geographical Society, London.
Barbosa A, Moreno E. 1999. Hindlimb morphology and locomotion performance in waders: an evolutionary approach. Biol J Linn Soc. 67: 313–330.
Birn-Jeffery AV, Miller CE, Naish D et al. 2012. Pedal claw curvature in birds, compensating for mass-specific and phylogenetic control. PLoS One. doi:10.1371/journal.pone.0050555
Dilger WC. 1956. Adaptive modifications and ecological isolating mechanism in the thrush genera Catharus and Hylocichla. Wilson Bull. 68: 171–199.
De souza O, Schoereder JH, Brown V et al. 2001. A theoretical overview of the processes determining species richness in forest fragment. In: Bierregaard RO Jr, Gascon C, Lovejoy TE, Mesquita R (eds). Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest. Yale Univ. Press, New Haven, London.
Dehling DM, Jordano P, Schaefer HM et al. 2016. Morphology predicts species’ functional roles and their degree of specialization in plant-frugivore interactions. PROY SOC B BIOL SCI. doi.org/10.1098/rspb.2015.2444
Grant PR. 1965. The adaptive significance of some size trends in Island birds. Evolution 19: 355–367.
Grant PR. 1971. Variation in the tarsus length of birds in island and mainland regions. Evolution 25: 599–614.
Grant PR. 1986. Bill size, body size, and the ecological adaptation of bird species to competitive situations on island. Syst. Zool. 17: 319–333.
Greenberg R. 1989. Neophobia, aversion to open space, and ecological plasticity in song and swamp sparrows. Can. J. Zool. 67: 1194–1199.
Garnier E, Cortez J, Billes G et al. 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecological Society of America. 85: 2630–2637.
Gilroy J, Uribe CAM, Haugaasen T et al. 2014. Effect of scale on trait predictor of species responses to agriculture. Conserv Biol. 29: 463–472.
Glomvinya S, Tantasirin C, Tongdeenok P et al. 2016. Change in rainfall characteristics at Huai Kog-Ma watershed, Chiang Mai Province. Thai J For. 35: 66–77.
James FC. 1982. The ecological morphology of birds: a review. Animal. Zoologici Fennici. 19: 265–275.
Karr JR, Freemark KE. 1983. Habitat selection and environmental gradients: dynamics in the “stable” tropics. Ecological Society of America. 64: 1481–1494.
Kováts D, Harnos A. 2005. Morphological classification of conspecific birds from closely situated breeding areas – A case study of the Common Nightingale. Ornis Hung. 23(2): 20–30.
McNamara JM, Houston AI. 1990. The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheor. 38(1): 37–61.
MacLeod MG, Valentine J, Cowan A, Wade A, McNeil L, Bernard K. 2008. Metabolisable energy yield from a range of varieties in broilers, cockerels and turkeys. Br. Poult. Sci. 49: 368–377.
Marod D, Kutintara U. 2009. Forest Ecology. Faculty of Forestry, Kasetsart University. Bangkok.
Marod D, Sungkaew S, Duengkae P, et al. 2014. Plant diversity of lower montane evergreen forest at Huai Kogma watershed area, Doi Suthep-Pui National Park, Chiang Mai province. In: Marod D, Thapyai C (eds) Thai forest ecological research network, T-FERN ecological knowledge for sustainable management. Naresuan University, 22-23 January 2015. [Thailand]
Nussey DH, Wilson AJ, Brommer JE. 2007. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20: 831–844.
Newbold T, Scharlemann JPW, Butchart SHH et al. 2012. Ecological traits affect the response of tropical forest bird species to land-use intensity. Proc. R. Soc. Lond. doi: 10.1098/rspb.2012.2131
Osterhaus MB. 1962. Modifications in the leg structure of some North American Warblers. Am Midl Nat. 68: 474–486.
Payne RB, Risley CJ. 1976. Systematics and evolutionary relationships among the Heron (Ardeidae). Museum of Zoology, University of Michigan, Michigan.
Pfenning DW, Wund MA, Snell-Rood EC et al. 2010. Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol. 25: 459–467.
Powell LL, Stouffer PC, Johnson ET. 2013. Recovery of understory bird movement across the interface of primary and secondary Amazon rainforest. Auk. 130: 459–468.
Powell T, Norbert J, Cordeiro J, Stratford A. 2015. Ecology and conservation of avian insectivores of the rainforest understory: a pantropical perspective. Biol. Conserv. 188: 1–10.
Phillips HRP, Newbold T, Purvis A. 2017. Land-use effect on local biodiversity in tropical forests vary between continents. Biodivers Conserv. 26: 2251–2270.
Pratumtong D, Gale GA, Duengkae P, Pongpattananurak N, Chimchome V. 2018. The influence of environmental variables on bird communities in tropical seasonal forests, western Thailand. JWT. 25: 49–65.
Richardson F. 1942. Adaptive modification for tree-trunk foraging in birds. Univ. Calif. publ. zool. 46: 317–368.
Raffaelli DG, Frid CLJ. 2010. Ecosystem Ecology: A New Synthesis. Cambridge University Press, Cambridge.
Round PD, Andrew JP, Wangworn S, George AG. 2011. The avifauna of the Mo Singto forest dynamics plot, Khao Yai National Park, Thailand. Nat. Hist. Bull. Siam. Soc. 57: 57-80.
R Core Team. 2014. R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria.
Rolo V, Olivier PI, van Aarde R. 2017. Tree and bird functional groups as indicators of recovery at generating subtropical coastal dune forest. Restor. Ecol. 25: 788–797.
Storer RW. 1960. Adaptive radiation in birds. In: Marshall A.J. ed. Biology and comparative physiology of birds, Vol 1. Academic Press, New York.
Schulenberg TS. 1983. Foraging behavior, eco-morphology, and systematic of some antshrikes (Formicariidae: Thamnomanse). Wilson bull. 95: 505–521.
Stratford JA, Stouffer PC. 1999. Local extinctions of terrestrial insectivorous birds in a fragmented landscape near Manaus, Brazil. Conserv Biol. 13: 1416–1423.
Schliemann SA, Bockheim JG. 2011. Methods for studying treefall gaps: a review. For. Ecol. Manag. 261: 1143–1151.
Siri S, Duengkae P, Marod D. 2013. Species diversity and abundance of birds in hill evergreen forest permanent plot at Huai Kok Ma, Chiang Mai province. JWT. 20: 97–112.
Sreekar R, Srinivasan U, Mammides C et al. 2015. The effect of land-use on the diversity and mass-abundance relationships of understory avian insectivores in Sri Lanka and southern India. Sci. Rep. 5: 11569 DOI: 10.1038/srep11569
Stratford JA, Stouffer PC. 2015. Forest fragmentation alters microhabitat availability for neotropical terrestrial insectivore birds. Biol. Conserv. 188: 109–115.
Shao S, Quan Q, Cai S, Qu Y, Lei F. 2016. Evolution of body morphology and beak shape revealed by a morphometric analysis of 14 Paridae species. Front Zool. 13: 30. doi.org/10.1186/s12983-016-0162-0
Shatkovska OV, Ghazali M. 2017. Relationship between developmental modes, flight styles and wing morphology in birds. European Journal of Zoological Research. 84: 390–401.
Siri S, Ponpituk Y, Safoowong M, Marod D, Duengkae P. 2019. The natural forest gaps maintenance diversity of understory birds in Mae Sa-Kog Ma Biosphere Reserve, northern Thailand. Biodiversitas 20: 181–189.
Srinivasan U. 2019. Morphological and behavioral correlates of long-term bird survival in selectively logged forest. Front Ecol Evol. 7:17. doi: 10.3389/fevo.2019.00017
Thiollay JM. 1992. Influence of selective logging on bird species diversity in a Guianan rain forest. Conserv Biol. 6: 47–63.
Thuiller W, Pironon S, Psomas A et al. 2014. The European functional tree of bird life in the face of global change. Nat. Commun. 5: 3118. DOI: 10.1038/ncomms4118
Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E. 2007. Let the concept of trait be functional!. Oikos 116: 882–892.
Vu LV. 2009. Diversity and similarity of butterfly communities in five different habitat types at Tam Dao National Park, Vietnam. J. Zool. 277: 15–22.
Winkler H, Bock W. 1976. Analyse der Kräfteverhältnisse bei Klettervögeln. J. Ornithol. 117: 397–418.
Whelan CJ. 2001. Foliage structure influences foraging of insectivorous forest bird: an experimental study. Ecological Society of America. 82: 219–231.
Walther BA. 2002. Vertical stratification and use of vegetation and light habitat by Neotropical forest birds. J. Ornithol. 143: 64–81.
Wunderle JM, Willig RMR, Henriques LMP. 2005. Avian distribution in treefall gaps and understorey of terra firme forest in the lowland Amazon. Ibis. 147: 109–129.
Werema C. 2015. Seasonal variation in understory bird species diversity and abundance in the Uluguru Nature Reserve, Tanzania. Afr. J. Ecol. 54: 299–307.
Xing L, Jingmai K, Connor Q et al. 2019. A new enantiornithine bird with unusual pedal proportions found in amber. Curr Biol. 29(14): 2396–2401.
Zeffer A, Johansson LC, Marmebro A. 2003. Functional correlation between habitat use and leg morphology in birds (Aves). Biol J Linn Soc. 79: 461–481.
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