Abstract
Species can compete both directly via aggressive encounters (interference) and indirectly through their shared use of a limited resource (exploitation). Depending on the circumstances interference, exploitation, and their interplay can either lead to competitive exclusion or drive niche partitioning to maintain species coexistence. Thus, understanding species coexistence in nature requires accurately identifying the mechanisms that contribute to competition among the species in question. In the southern United States, the native lizard Anolis carolinensis becomes more arboreal in the presence of the invasive Anolis sagrei, resulting in highly consistent vertical habitat partitioning where the species co-occur. These species have been thought to largely ignore each other and engage only in exploitative competition for shared arthropod prey. To test for the presence and consequences of direct interference, we conducted behavioral trials in the field, introducing a heterospecific male intruder to individuals of both species. We find that interference competition is asymmetric in favor of A. sagrei, which are more likely to display and less likely to retreat than A. carolinensis. Concordant with their arboreal tendencies, male A. carolinensis also trend toward retreating upward more often than expected by chance. These asymmetries are prevalent despite the almost complete absence of physical attacks, suggesting that interspecific signaling and avoidance behavior by A. carolinensis resolve most potential conflicts before they escalate to combat. Our results highlight the potential for direct interference more subtle than frequent outright combat to structure communities, and Anolis assemblages in particular.
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References
Adams DC (2004) Character displacement via aggressive interference in Appalachian salamanders. Ecology 85:2664–2670. https://doi.org/10.1890/04-0648
Amarasekare P (2002) Interference competition and species coexistence. Proc R Soc Lond B Biol Sci 269:2541–2550. https://doi.org/10.1098/rspb.2002.2181
Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122. https://doi.org/10.1046/j.1461-0248.2003.00530.x
Armstrong RA, McGehee R (1976) Coexistence of species competing for shared resources. Theor Popul Biol 9:317–328. https://doi.org/10.1016/0040-5809(76)90051-4
Armstrong RA, McGehee R (1980) Competitive Exclusion. Am Nat 115:151–170. https://doi.org/10.1086/283553
Blaustein AR, Risser AC (1976) Interspecific interactions between three sympatric species of kangaroo rats (Dipodomys). Anim Behav 24:381–385. https://doi.org/10.1016/S0003-3472(76)80047-4
Blumstein DT, Daniel JC, Evans CS (2006) JWatcher™ 1.0: An introductory user’s guide https://www.reed.edu/biology/courses/BIO342/2010_syllabus/2010_labs/week1_stuff/JW1manual.pdf. Accessed 20 Sept 2017
Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239. https://doi.org/10.1890/0012-9658(2000)081%5b1225:cbtesi%5d2.0.co;2
Calsbeek R (2009) Sex-specific adult dispersal and its selective consequences in the brown anole, Anolis sagrei. J Anim Ecol 78:617–624. https://doi.org/10.1111/j.1365-2656.2009.01527.x
Campbell TS (2000) Analysis of the effects of an exotic lizard (Anolis sagrei) on a native lizard (Anolis carolinensis) in Florida, using islands as experimental units. PhD dissertation, Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee, USA
Carothers JH, Jaksić FM (1984) Time as a niche difference: the role of interference competition. Oikos 42:403–406. https://doi.org/10.2307/3544413
Case TJ, Gilpin ME (1974) Interference competition and niche theory. Proc Natl Acad Sci 71:3073–3077. https://doi.org/10.1073/pnas.71.8.3073
Chesson P (1991) A need for niches? Trends Ecol Evol 6:26–28. https://doi.org/10.1016/0169-5347(91)90144-M
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. https://doi.org/10.1146/annurev.ecolsys.31.1.343
Chock RY, Shier DM, Grether GF (2018) Body size, not phylogenetic relationship or residency, drives interspecific dominance in a little pocket mouse community. Anim Behav 137:197–204. https://doi.org/10.1016/j.anbehav.2018.01.015
Chucholl C, Stich HB, Maier G (2008) Aggressive interactions and competition for shelter between a recently introduced and an established invasive crayfish: Orconectes immunis vs. O. limosus. Fundam Appl Limnol Arch Hydrobiol 172:27–36. https://doi.org/10.1127/1863-9135/2008/0172-0027
Collette BB (1961) Correlations between ecology and morphology in anoline lizards from Havana, Cuba, and southern Florida. Bull Mus Comp Zool Harvard 125:135–162
Connell JH (1983) On the prevalence and relative importance of interspecific competition: evidence from field experiments. Am Nat 122:661–696. https://doi.org/10.1086/284165
Dufour CMS, Herrel A, Losos JB (2018) The effect of recent competition between the native Anolis oculatus and the invasive A. cristatellus on display behavior. PeerJ 6:e4888. https://doi.org/10.7717/peerj.4888
Edwards JR, Lailvaux SP (2012) Display behavior and habitat use in single and mixed populations of Anolis carolinensis and Anolis sagrei Lizards. Ethology 118:494–502. https://doi.org/10.1111/j.1439-0310.2012.02037.x
Edwards JR, Lailvaux SP (2013) Do interspecific interactions between females drive shifts in habitat use? A test using the lizards Anolis carolinensis and A. sagrei. Biol J Linn Soc Lond 110:843–851. https://doi.org/10.1111/bij.12180
Freshwater C, Ghalambor CK, Martin PR (2014) Repeated patterns of trait divergence between closely related dominant and subordinate bird species. Ecology 95:2334–2345. https://doi.org/10.1890/13-2016.1
Glossip D, Losos JB (1997) Ecological correlates of number of subdigital lamellae in anoles. Herpetologica 53:192–199
Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15. https://doi.org/10.1017/S0094837300004310
Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev 84:617–635. https://doi.org/10.1111/j.1469-185X.2009.00089.x
Grether GF, Anderson CN, Drury JP, Kirschel ANG, Losin N, Okamoto K, Peiman KS (2013) The evolutionary consequences of interspecific aggression. Ann N Y Acad Sci 1289:48–68. https://doi.org/10.1111/nyas.12082
Grether GF, Peiman KS, Tobias JA, Robinson BW (2017) Causes and consequences of behavioral interference between species. Trends Ecol Evol 32:760–772. https://doi.org/10.1016/j.tree.2017.07.004
Herrmann NC, Yates SS, Fredette JR, Leavens MK, Moretti R, Reynolds RG (2018) Lizards on islands within islands: microhabitat use, movement, and cannibalism in Anolis sagrei (Brown Anole) and Anolis smaragdinus (Bahamas Green Anole). Carib Nat 50:1–17
Hess NE, Losos JB (1991) Interspecific aggression between Anolis cristatellus and A. gundlachi: comparison of sympatric and allopatric populations. J Herpetol 25:256–259. https://doi.org/10.2307/1564669
Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14:328–330. https://doi.org/10.1016/S0169-5347(99)01636-5
Hongo Y, Okamoto K (2013) Interspecific contests between males of two Japanese stag beetle species, Lucanus maculifemoratus and Prosopocoilus inclinatus: what overcomes a body size disadvantage? Behaviour 150:39–59. https://doi.org/10.1163/1568539X-00003036
Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105:405–412. https://doi.org/10.1007/BF00328744
Jenssen TA, Nunez SC (1998) Spatial and breeding relationships of the Lizard, Anolis carolinensis: evidence of intrasexual selection. Behaviour 135:981–1003
Jenssen TA, Marcellini DL, Pague CA, Jenssen LA (1984) Competitive Interference between the Puerto Rican Lizards, Anolis cooki and A. cristatellus.. Copeia 1984:853–862. https://doi.org/10.2307/1445328
Kamath A, Losos JB (2017) The erratic and contingent progression of research on territoriality: a case study. Behav Ecol Sociobiol 71:89. https://doi.org/10.1007/s00265-017-2319-z
Kamath A, Losos JB (2018) Estimating encounter rates as the first step of sexual selection in the lizard Anolis sagrei. Proc R Soc B 285:20172244. https://doi.org/10.1098/rspb.2017.2244
Kamath A, Stuart YE, Campbell TS (2013) Behavioral Partitioning by the native lizard Anolis carolinensis in the presence and absence of the invasive Anolis sagrei in Florida. Breviora. https://doi.org/10.3099/mcz8.1
Kaufmann JH (1983) On the definitions and functions of dominance and territoriality. Biol Rev 58:1–20. https://doi.org/10.1111/j.1469-185X.1983.tb00379.x
Kimura K, Chiba S (2010) Interspecific interference competition alters habitat use patterns in two species of land snails. Evol Ecol 24:815–825. https://doi.org/10.1007/s10682-009-9339-8
King W, Krakauer T (1966) The exotic herpetofauna of southeast Florida. Quart J Fla Acad Sci 29:144–154
Lach L (2005) Interference and exploitation competition of three nectar-thieving invasive ant species. Insectes Soc 52:257–262. https://doi.org/10.1007/s00040-005-0807-z
Lawton JH, Hassell MP (1981) Asymmetrical competition in insects. Nature 289:793–795. https://doi.org/10.1038/289793a0
Leal M, Rodríguez-Robles JA, Losos JG (1998) An experiment study of interspecific interactions between two Puerto Rican Anolis lizards. Oecologia 117:273–278. https://doi.org/10.1007/s004420050658
Leibold MA (1995) The niche concept revisited: mechanistic models and community context. Ecology 76:1371–1382. https://doi.org/10.2307/1938141
Lister BC (1976) The nature of niche expansion in West Indian Anolis lizards I: ecological consequences of reduced competition. Evolution 30:659–676. https://doi.org/10.2307/2407808
Losin N (2012) The evolution and ecology of interspecific territoriality: Studies of Anolis lizards and North American wood-warblers. PhD dissertation, Department of Ecology and Evolutionary Biology, UCLA, Los Angeles, California, USA
Losos JB (1990) Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecol Monogr 60:369–388. https://doi.org/10.2307/1943062
Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, Berkeley
Losos JB, Sinervo B (1989) The effects of morphology and perch diameter on sprint performance of Anolis lizards. J Exp Biol 145:23–30
Mikami OK, Kawata M (2004) Does interspecific territoriality reflect the intensity of ecological interactions? A theoretical model for interspecific territoriality. Evol Ecol Res 6:765–775
Morin PJ, Johnson EA (1988) Experimental studies of asymmetric competition among Anurans. Oikos 53:398–407. https://doi.org/10.2307/3565542
Morse DH (1974) Niche breadth as a function of social dominance. Am Nat 108:818–830. https://doi.org/10.1086/282957
Oliveira JCF, de Castro TM, Vrcibradic D, Drago MC, Prates I (2018) A second Caribbean anole lizard species introduced to Brazil. Herpetol Notes 11:761–764
Ord TJ, Stamps JA (2009) Species identity cues in animal communication. Am Nat 174:585–593. https://doi.org/10.1086/605372
Ord TJ, King L, Young AR (2011) Contrasting theory with the empirical data of species recognition. Evolution 65:2572–2591. https://doi.org/10.1111/j.1558-5646.2011.01319.x
Peiman KS, Robinson BW (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85:133–158. https://doi.org/10.1086/652374
Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266. https://doi.org/10.1086/284413
Powell R, Henderson RW, Farmer MC, Breuil M, Echternacht AC, van Buurt G, Romagosa CM, Perry G (2011) Introduced amphibians and reptiles in the Greater Caribbean. In: Hailey A, Wilson BS, Horrocks JA (eds) Conservation of Caribbean Island Herpetofaunas, vol 1. Brill, Leiden, pp 49–138
R Development Core Team (2017) R: A language and environment for statistical computing. Austria, Vienna
Rasband WS (1997) ImageJ. US National Institutes of Health, Bethesda
Reedy AM, Pope BD, Kiriazis NM, Giordano CL, Sams CL, Warner DA, Cox RM (2017) Female anoles display less but attack more quickly than males in response to territorial intrusions. Behav Ecol 28:1323–1328. https://doi.org/10.1093/beheco/arx095
Reynolds HL, Rajaniemi TK (2007) Plant interactions: competition. In: Pugnaire F, Valladares F (eds) Functional plant ecology. CRC Press, Boca Raton, pp 457–480
Robinson SK, Terborgh J (1995) Interspecific aggression and habitat selection by Amazonian birds. J Anim Ecol 64:1–11. https://doi.org/10.2307/5822
Rowell TE (1966) Hierarchy in the organization of a captive baboon group. Anim Behav 14:430–443. https://doi.org/10.1016/S0003-3472(66)80042-8
Rowell TE (1974) The concept of social dominance. Behav Biol 11:131–154. https://doi.org/10.1016/S0091-6773(74)90289-2
Rychlik L, Zwolak R (2006) Interspecific aggression and behavioural dominance among four sympatric species of shrews. Can J Zool 84:434–448. https://doi.org/10.1139/z06-017
Savage JM, Bolaños F (2009) A checklist of the amphibians and reptiles of Costa Rica: additions and nomenclatural revisions. Zootaxa 2005:1–23
Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New York
Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726. https://doi.org/10.2307/1935534
Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39. https://doi.org/10.1126/science.185.4145.27
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizard species. Ecol Monogr 45:233–258. https://doi.org/10.2307/1942423
Schoener TW (1983) Field experiments on interspecific competition. Am Nat 22:240–285. https://doi.org/10.1086/284133
Schoener TW (1986) Resource partitioning. In: Kikkawa J, Anderson DJ (eds) Community ecology: pattern and process. Blackwell Scientific, Melbourne, pp 91–126
Schoener TW, Schoener A (1971) Structural habitats of West Indian Anolis lizards. I. Lowland Jamaica. Breviora 368:1–53
Schoener TW, Schoener A (1982) Intraspecific variation in home-range size in some Anolis lizards. Ecology 63:809–823. https://doi.org/10.2307/1936801
Shelley EL, Tanaka MYU, Ratnathicam AR, Blumstein DT (2004) Can Lanchester’s laws help explain interspecific dominance in birds? Condor 106:395–400
Stamps JA (1977) The relationship between resource competition, risk, and aggression in a tropical territorial lizard. Ecology 58:349–358. https://doi.org/10.2307/1935609
Stamps JA (1978) A field study of the ontogeny of social behavior in the lizard Anolis aeneus. Behaviour 66:1–30. https://doi.org/10.1163/156853978X00396
Stuart YE, Losos JB (2013) Ecological character displacement: glass half full or half empty? Trends Ecol Evol 28:402–408. https://doi.org/10.1016/j.tree.2013.02.014
Stuart YE, Campbell TS, Hohenlohe PA, Reynolds RG, Revell LJ, Losos JB (2014) Rapid evolution of a native species following invasion by a congener. Science 346:463–466. https://doi.org/10.1126/science.1257008
Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton
Tokarz RR, Beck JW Jr (1987) Behaviour of the suspected lizard competitors Anolis sagrei and Anolis carolinensis: an experimental test for behavioural interference. Anim Behav 35:722–734. https://doi.org/10.1016/S0003-3472(87)80108-2
Turnbough N (2016) Assessing the functional similarity of native and invasive Anolis lizards in the food webs of structurally-simple habitats in Florida. PhD dissertation, Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee, USA
Ziv Y, Abramsky Z, Kotler BP, Subach A (1993) Interference competition and temporal and habitat partitioning in two gerbil species. Oikos 66:237–246. https://doi.org/10.2307/3544810
Acknowledgements
This work would not have been possible without the logistical and intellectual support provided by Irene Arpayoglou and staff at the Indian River Lagoon Aquatic Preserve. We thank Carol Herzog, Dylan Gavagni, and staff at the St. Sebastian River Preserve for providing lodging. We also thank Jonathan Losos, Ambika Kamath, and Elizabeth Wolkovich for providing helpful feedback on the manuscript.
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This study was generously funded by the Harvard Museum of Comparative Zoology, Harvard Center for the Environment, and Harvard College Research Program.
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NCH conceived the study. KAC analyzed videos. KAC and NCH jointly designed the experiment, conducted fieldwork, analyzed data, constructed figures, and wrote the manuscript.
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Culbertson, K.A., Herrmann, N.C. Asymmetric interference competition and niche partitioning between native and invasive Anolis lizards. Oecologia 190, 811–820 (2019). https://doi.org/10.1007/s00442-019-04466-1
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DOI: https://doi.org/10.1007/s00442-019-04466-1