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A new perspective on size hierarchies in nature: patterns, causes, and consequences

  • Behavioral Ecology
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Abstract

Many plant and animal aggregations have size hierarchies within which a variety of sizes of individuals, from large to small, can be found. Size hierarchies are thought to indicate the existence of competition amongst individuals within the aggregation, but determining their exact cause is difficult. The key to understanding size hierarchies lies in first quantifying the pattern of size and growth of individuals. We conducted a quantitative investigation of pattern in the size hierarchy of the clown anemonefish Amphiprion percula, in Madang Lagoon, Papua New Guinea. Here, groups of A. percula occupy sea anemones (Heteractis magnifica) that provide protection from predators. Within each anemone there is a single group composed of a breeding pair and zero to four non-breeders. Within each group there is a single size hierarchy; the female is largest (rank 1), the male is second largest (rank 2), and the non-breeders get progressively smaller (ranks 3–6). We demonstrate that individuals adjacent in rank are separated by body size ratios whose distribution is significantly different from the distribution expected under a null model—the growth of individuals is regulated such that each dominant ends up being about 1.26 times the size of its immediate subordinate. We show that it is decisions about growth at the individual level that generate the size hierarchy at the group level, and thereby determine maximum group size and population size. This study provides a new perspective on the pattern, causes and consequences of size hierarchies.

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References

  • Allee WC, Greenberg B, Rosenthal GM, Frank P (1948) Some effects of social organization on growth in the green sunfish, Lepomis cyanellus. J Exp Zool 108:1–9

    Article  PubMed  CAS  Google Scholar 

  • Allen GR (1972) The anemonefishes: their classification and biology, 2nd edn. T.F.H., Neptune City

    Google Scholar 

  • Ballare CL, Scopel AL (1997) Phytochrome signaling in plant canopies: testing its population level implications with photoreceptor mutants of Arabidopsis. Funct Ecol 11:441–450

    Article  Google Scholar 

  • Ballare CL, Scopel AL, Sanchez RA (1990) Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247:329–332

    Article  PubMed  CAS  Google Scholar 

  • Balshine-Earn S, Neat FC, Reid H, Taborsky M (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav Ecol 9:432–438

    Article  Google Scholar 

  • Balshine S, Leach B, Neat F, Reid H, Taborsky M, Werner N (2001) Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav Ecol Sociobiol 50:134–140

    Article  Google Scholar 

  • Barlow GW, Rogers W, Fraley N (1986) Do Midas cichlids win through prowess or daring? It depends. Behav Ecol Sociobiol 19:1–8

    Article  Google Scholar 

  • Begon M (1984) Density and individual fitness: asymmetric competition. In: Shorrocks B (ed) Evolutionary ecology. Blackwell, London, pp 175–194

    Google Scholar 

  • Booth DJ (1995) Juvenile groups in a coral-reef damselfish: density-dependent effects on individual fitness and population demography. Ecology 76:91–106

    Article  Google Scholar 

  • Brown ME (1946) The growth of brown trout (Salmo trutta Linn.). I. Factors influencing the growth of trout fry. J Exp Biol 22:118–129

    Google Scholar 

  • Brunkow PE, Collins JP (1998) Group structure affects patterns of aggression in larval salamanders. Behav Ecol 9:508–514

    Article  Google Scholar 

  • Buston PM (2002) Group structure of the clown anemonefish, Amphiprion percula. PhD dissertation, Cornell University

  • Buston PM (2003a) Size and growth modification in clownfish. Nature 424:145–146

    Article  CAS  Google Scholar 

  • Buston PM (2003b) Forcible eviction and prevention of recruitment in the clown anemonefish. Behav Ecol 14:576–582

    Article  Google Scholar 

  • Buston PM (2003c) Mortality is associated with social rank in the clown anemonefish (Amphiprion percula). Mar Biol 143:811–815

    Article  Google Scholar 

  • Buston PM (2004a) Territory inheritance in the clown anemonefish. Proc R Soc Ser B 271 [Suppl]:S252–S254

    Article  Google Scholar 

  • Buston PM (2004b) Does the presence of non-breeders enhance the fitness of breeders? An experimental analysis in the clown anemonefish. Behav Ecol Sociobiol 57:23–31

    Article  Google Scholar 

  • Caillet GM, Love MS, Ebeling AW (1986) Fishes: a field and laboratory manual on the structure, identification, and natural history. Wadsworth, Belmont

    Google Scholar 

  • Cant MA, Llop JB, Field J (2006) Individual variation in social aggression and the probability of inheritance: theory and a field test. Am Nat 167:837–852

    Article  Google Scholar 

  • Coates D (1980) Prey-size intake in humbug damselfish, Dascyllus aruanus (Pisces, Pomacentridae) living within social groups. J Anim Ecol 49:335–340

    Article  Google Scholar 

  • Donaldson TJ (1989) Facultative monogamy in obligate coral dwelling hawkfishes (Cirrhitidae). Environ Biol Fish 26:295–302

    Article  Google Scholar 

  • Elliott JK, Mariscal RN (2001) Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment. Mar Biol 138:23–36

    Article  Google Scholar 

  • Elliott JK, Elliott JM, Mariscal RN (1995) Host selection, location, and association behaviors of anemonefishes in field settlement experiments. Mar Biol 122:377–389

    Article  Google Scholar 

  • Falster DS, Westoby M (2003) Plant height and evolutionary games. Trees 18:337–343

    Google Scholar 

  • Fautin DG (1992) Anemonefish recruitment: the roles of order and chance. Symbiosis 14:143–160

    Google Scholar 

  • Field J, Shreeves G, Sumner S (1999) Group size, queuing, and helping decisions in facultatively eusocial hover wasps. Behav Ecol Sociobiol 45:378–385

    Article  Google Scholar 

  • Forrester GE (1990) Factors influencing the juvenile demography of a coral reef fish. Ecology 71:1666–1681

    Article  Google Scholar 

  • Forrester GE (1991) Social rank, individual size, and group composition as determinants of food consumption by humbug damselfish, Dascyllus aruanus. Anim Behav 42:701–711

    Article  Google Scholar 

  • Fox HE, White SA, Kao MHF, Fernald RD (1997) Stress and dominance in a social fish. J Neurosci 17:6453–6469

    Google Scholar 

  • Franco M (1986) The influence of neighbours on the growth of modular organisms with an example from trees. Philos Trans R Soc Lond Ser B Biol Sci 313:209–225

    Article  Google Scholar 

  • Fricke H (1974) Oko-ethologie des monogamen Anemonefisches Amphiprion bicinctus (Freiwasseruntersuchung aus dem Roten Meer). Z Tierpsychol 32:225–256

    Google Scholar 

  • Fricke HW (1979) Mating system, resource defense and sex change in the anemonefish Amphiprion akallopisos. Z Tierpsychol 50:313–326

    Google Scholar 

  • Fricke H, Fricke S (1977) Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266:830–832

    Article  PubMed  CAS  Google Scholar 

  • Geber MA (1989) Interplay of morphology and development on size inequality: a Poygonum greenhouse study. Ecol Monogr 59:267–288

    Article  Google Scholar 

  • Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution Press, Washington, D.C.

    Google Scholar 

  • Hattori A (1991) Socially controlled growth and size-dependent sex change in the anemonefish Amphiprion frenatus in Okinawa, Japan. Jpn J Ichthyol 38:165–177

    Google Scholar 

  • Hattori A (1994) Inter-group movement and mate acquisition tactics of the protandrous anemonefish, Amphiprion clarkii, on a coral reef, Okinawa. Jpn J Ichthyol 41:159–165

    Google Scholar 

  • Heg D, Bender N, Hamilton I (2004) Strategic growth decisions in helper cichlids. Proc R Soc Lond Ser B 271 [Suppl]:S505–S508

    Article  Google Scholar 

  • Hobbs JPA, Munday PL (2004) Intraspecific competition controls spatial distribution and social organization of the coral-dwelling goby Gobiodon histrio. Mar Ecol Prog Ser 278:253–259

    Article  Google Scholar 

  • Hofman HA, Fernald RD (2000) Social status controls somatostatin neuron size and growth. J Neurosci 20:4740–4744

    Google Scholar 

  • Holbrook SJ, Schmitt RJ (2005) Growth, reproduction, and survival of a tropical sea anemone (Actinaria): benefits of hosting anemonefish. Coral Reefs 24:67–73

    Article  Google Scholar 

  • Horn HS, May RM (1977) Limits to similarity among coexisting competitors. Nature 270:660–661

    Article  Google Scholar 

  • Hutchinson GE (1959) Homage to Santa Rosalia, or why are there so many kinds of animals. Am Nat 93:145–159

    Article  Google Scholar 

  • Jebb MHP, Lowry JK (1995) Natural history of Madang Lagoon with an appendix of collecting localities. Rec Aust Mus 22 [Suppl]:1–24

    Google Scholar 

  • Jones GP (1987) Competitive interactions among adults and juveniles in a coral reef fish. Ecology 68:1534–1547

    Article  Google Scholar 

  • Jones M, Harper JL (1987a) The influence of neighbours on the growth of trees. I. the demography of buds in Betula pendula. Proc R Soc Lond Ser B Biol Sci 232:1–18

    Article  Google Scholar 

  • Jones M, Harper JL (1987b) The influence of neighbours on the growth of trees. II. the fate of buds on long and short shoots in Betula pendula. Proc R Soc Lond Ser B Biol Sci 232:19–33

    Google Scholar 

  • Keough JJ, Downes BJ (1982) Recruitment of marine invertebrates: the role of active larval choices and early mortality. Oecologia 54:348–352

    Article  Google Scholar 

  • Koebele BP (1985) Growth and the size hierarchy effect: an experimental assessment of three proposed mechanisms; activity differences, disproportional food acquisition, physiological stress. Environ Biol Fish 12:181–188

    Article  Google Scholar 

  • Kokko H, Johnstone R (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Biol Sci Ser B 266:571–578

    Article  Google Scholar 

  • Kuwamura T, Yogo Y, Nakashima Y (1994) Population dynamics of goby Paragobiodon echinocephalus and host coral Stylophora pistillata. Mar Ecol Prog Ser 103:17–23

    Article  Google Scholar 

  • Lassig BR (1976) Field observations on the reproductive behaviour of Paragobiodon spp. (Osteichthyes Gobiidae) at Heron Island Great Barrier Reef. Mar Behav Physiol 3:283–293

    Article  Google Scholar 

  • Lassig BR (1977) Socioecological strategies adopted by obligate coral-dwelling fishes. In: Proceedings of the 3rd International Coral Reef Symposium, pp 565–570

  • MacArthur R, Levins R (1967) The limiting similarity, convergence and divergence of coexisting species. Am Nat 101:377–385

    Article  Google Scholar 

  • Magnusson JJ (1962) An analysis of aggressive behavior, growth, and competition for food and space in medaka [Oryzias latipes (Pisces, Cyprinodontidae)]. Can J Zool 40:313–363

    Article  Google Scholar 

  • Mahall BE, Callaway RM (1991) Root communication among desert shrubs. Proc Natl Acad Sci USA 88:874–876

    Article  PubMed  CAS  Google Scholar 

  • Mahall BE, Callaway RM (1992) Root communication mechanisms and intracommunity distributions of two desert shrubs. Ecology 73:2145–2151

    Article  Google Scholar 

  • Mariscal RN (1970) The nature of the symbiosis between Indo-Pacific anemonefishes and sea anemones. Mar Biol 6:58–65

    Article  Google Scholar 

  • Marks PL, Gardescu S (1998) A case study of sugar maple (Acer saccharum) as a forest seedling bank species. J Torrey Bot Soc 125:287–296

    Article  Google Scholar 

  • Mayr E (1961) Cause and effect in biology. Science 134:1501–1506

    Article  PubMed  CAS  Google Scholar 

  • Mitchell JS (2005) Queue selection and switching by false clown anemonefish, Amphiprion ocellaris. Anim Behav 69:643–652

    Article  Google Scholar 

  • Mitchell JS, Dill LM (2005) Why is group size correlated with the size of the host sea anemone in the false clown anemonefish? Can J Zool 83:372–376

    Article  Google Scholar 

  • Moyer JT, Nakazano A (1978) Protandrous hermaphroditism in six species of the anemonefish genus Amphiprion in Japan. Jpn J Ichthyol 25:101–106

    Google Scholar 

  • Nagashima H, Terashima I, Katoh S (1995) Effects of plant density on frequency distributions on plant height in Chenopdium album stands: analysis based on continual monitoring of height growth of individual plants. Ann Bot 75:173–180

    Article  Google Scholar 

  • Nelson JS, Chou LM, Phang Violet PE (1994) Pigmentation variation in the anemonefish Amphiprion ocellaris (Teleostei: Pomacentridae): type, stability and its usefulness for individual identification. Raffles Bull Zool 42: 927–930

    Google Scholar 

  • Obeid M, Machin D, Harper JL (1967) Influence of density on plant to plant variation in fiber flax, Linum usitatissimum. Crop Sci 7:471–473

    Article  Google Scholar 

  • Ochi H (1986) Growth of the anemonefish Amphiprion clarkii in temperate waters, with special reference to the influence of settling time on the growth of 0-year olds. Mar Biol 92:223–229

    Article  Google Scholar 

  • Ochi H (1989) Acquisition of breeding space by non-breeders in the anemonefish Amphiprion clarkii in temperate waters of southern Japan. Ethology 83:279–294

    Article  Google Scholar 

  • Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth and survival. Hydrobiologia 530/531:513–520

    Article  Google Scholar 

  • Porat D, Chadwick-Furman NE (2005) Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthellae content and tissue regeneration. Mar Freshwater Behav Physiol 38:43–51

    Article  CAS  Google Scholar 

  • Poulson TL, Platt WJ (1996) Replacement patterns of beech and sugar maple in Warren Woods, Michigan. Ecology 77:1234–1253

    Article  Google Scholar 

  • Ragsdale JE (1999) Reproductive skew extended: the effect of resource inheritance on social organization. Evol Ecol Res 1:859–874

    Google Scholar 

  • Roff VL (1981) Constancy in the size ratios of sympatric species. Am Nat 118:394–404

    Article  Google Scholar 

  • Rose SM (1960) A feedback mechanism of growth control in tadpoles. Ecology 41:188–199

    Article  Google Scholar 

  • Ross RM (1978) Territorial behavior and ecology of the anemonefish Amphiprion melanopus on Guam. Z Tierpsychol 36:71–83

    Google Scholar 

  • Rowland WJ (1989) The effects of body size, aggression, and nuptial coloration on competition for territories in male threespine sticklebacks, Gasterosteus aculeatus. Anim Behav 37:282–289

    Article  Google Scholar 

  • Rubenstein DI (1981) Individual variation and competition in the everglades pygmy sunfish. J Anim Ecol 50:337–350

    Article  Google Scholar 

  • Schmitt RJ, Holbrook SJ (1999) Mortality of juvenile damselfish: implications for assessing processes that determine abundance. Ecology 80:35–50

    Google Scholar 

  • Shreeves G, Field J (2002) Group size and direct fitness in social queues. Am Nat 159:81–95

    Google Scholar 

  • Schwinning S (1996) Decomposition analysis of competitive symmetry and size structure dynamics. Ann Bot 77:47–57

    Article  Google Scholar 

  • Schwinning S, Weiner J (1998) Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113:447–455

    Article  Google Scholar 

  • Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619

    Article  Google Scholar 

  • Strong DR, Szyska LA, Simberloff DS (1979) Tests of community-wide character displacement against null hypotheses. Evolution 33:897–913

    Article  Google Scholar 

  • Sweatman HPA (1983) Influence of conspecifics on choice of settlement sites by larvae of two pomacentrid fishes (Dascyllus aruanus and Dascyllus reticulatus) on coral reefs. Mar Biol 75:225–229

    Article  Google Scholar 

  • Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236–1252

    Article  Google Scholar 

  • Tinbergen N (1964) On aims and methods of ethology. Z Tierpsychol 20:410–433

    Google Scholar 

  • Weiner J (1988) Variation in the performance of individuals in plant populations. In: Davy AJ, Hutchings MJ, Watkinson AR (eds) Plant population ecology. Blackwell, Oxford, pp 59–81

    Google Scholar 

  • Wiens JA (1981) Single-sample surveys of communities: are the revealed patterns real? Am Nat 117: 90–98

    Article  Google Scholar 

  • Williams DM, Sale PF (1981) Spatial and temporal patterns of recruitment of juvenile coral reef fishes to coral habitats within One Tree Lagoon, Great Barrier Reef. Mar Biol 65:245–253

    Article  Google Scholar 

  • Yamigashi H, Maruyama T, Mashiko K (1974) Social relation in small experimental population of Odonobutis obscurus (Temminck et Schlegel) as related to individual growth and food intake. Oecologia 17:187–202

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, Englewood Cliffs, N.J.

    Google Scholar 

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Acknowledgements

This work comprises a portion of P. M. B.’s doctoral thesis requirements (Cornell University). P. M. B. thanks his Ph.D. advisors, S. Emlen, P. Sherman, A. McCune, K. Reeve, and A. Bass for incredible support; J. Mizeu, M. Black, C. Norris, M. Moore, and the staffs of the Christensen Research Institute and the Jais Aben Resort for their assistance in Papua New Guinea; the landowners of Riwo village, the Madang Provincial Government, and the Papua New Guinea Government for permission to work on the reefs of Wongad, Sinub and Masamoz in Madang Lagoon. Further, we thank J. Dale, N. Hairston, F. Huntingford, D. Heg, J. von Fischer, L. Marschall, P. Munday, C. Petersen, R. Warner, C. Webb, M. Wong, and several anonymous reviewers for helpful comments and discussion. B. Ledvina (a.k.a. James Dean) helped with the Monte Carlo simulation. P. M. B. was supported by D. Christensen and the Christensen Fund, a National Science Foundation Doctoral Dissertation Improvement Grant, the Andrew W. Mellon Fund of the Cornell College of Agriculture and Life Sciences, the Cornell and National Chapters of Sigma Xi, the International Women’s Fishing Association, and the Cornell University Department of Neurobiology and Behavior. P. M. B. is currently funded by a Ramón y Cajal Fellowship of the Consejo Superior de Investigaciones Científicas. M. A. C. was supported by a Royal Commission for the Exhibition of 1851 Research Fellowship. M. A. C. is currently funded by a Royal Society University Research Fellowship.

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  1. Peter M. Buston

    Present address: Estación Biológica de Doñana, C.S.I.C., Avenida de María Luisa s/n., Pabellón de Perú, Apdo. 1056, 41013, Sevilla, Spain

  2. Michael A. Cant

    Present address: Department of Zoology, University of Cambridge, Downing Street, Cambridge , CB2 3EJ, UK

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  1. Department of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY, 14853, USA

    Peter M. Buston & Michael A. Cant

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Buston, P.M., Cant, M.A. A new perspective on size hierarchies in nature: patterns, causes, and consequences. Oecologia 149, 362–372 (2006). https://doi.org/10.1007/s00442-006-0442-z

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