1932

Abstract

Understanding what regulates population sizes of organisms with complex life cycles is challenging because limits on population sizes can occur at any stage or transition. We extend a conceptual framework to explore whether numbers of successfully laid eggs determine densities of later stages in insects, fish, amphibians, and snails inhabiting marine, freshwater, or terrestrial habitats. Our review suggests novel hypotheses, which propose characteristics of species or environments that create spatial variation in egg densities and predict when such patterns are maintained throughout subsequent life-cycle stages. Existing data, although limited, suggest that persistent, strong associations between egg and subsequent juvenile densities are likely for species where suitable egg-laying habitat is in short supply. Those associations are weakened in some environments and for some species by density-dependent losses of eggs or hatchlings. Such cross-ecosystem comparisons are fundamental to generality in ecology but demand place-based understandings of species’ biology and natural history.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-122420-102909
2021-11-03
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/52/1/annurev-ecolsys-122420-102909.html?itemId=/content/journals/10.1146/annurev-ecolsys-122420-102909&mimeType=html&fmt=ahah

Literature Cited

  1. Allen RM. 2014. Oviposition site influences dispersal potential in a marine bubble snail. Mar. Biol. Res. 10:515–22
    [Google Scholar]
  2. Alp M, Indermaur L, Robinson CT. 2013. Environmental constraints on oviposition of aquatic invertebrates with contrasting life cycles in two human-modified streams. Freshwat. Biol. 58:1932–45
    [Google Scholar]
  3. Beck MW. 1997. Inference and generality in ecology: current problems and an experimental solution. Oikos 78:265–73
    [Google Scholar]
  4. Bellile K, Vonesh J. 2016. Bioinsecticide and leaf litter combination increases oviposition and reduces adult recruitment to create an effective ovitrap for Culex mosquitoes. J. Vector Ecol. 41:123–27
    [Google Scholar]
  5. Billick I, Price MV 2010. The Ecology of Place: Contributions of Place-Based Research to Ecological Understanding Chicago, IL: Univ. Chicago Press
  6. Binckley CA, Resetarits WJ. 2002. Reproductive decisions under threat of predation: squirrel treefrog (Hyla squirella) responses to banded sunfish (Enneacanthus obesus). Oecologia 130:157–61
    [Google Scholar]
  7. Blaustein L, Kotler BP. 1993. Oviposition habitat selection by the mosquito Culiseta longiareolata: effects of conspecifics, food and green toad tadpoles. Ecol. Entomol. 18:104–8
    [Google Scholar]
  8. Bovill WD. 2013. The recruitment dynamics of stream insect larvae: oviposition and egg mortality of hydrobiosid caddisflies. PhD thesis University of Melbourne Melbourne, Australia:
    [Google Scholar]
  9. Bovill WD, Downes BJ, Lancaster J. 2013. A test of the preference–performance hypothesis with stream insects: Selective oviposition affects the hatching success of caddisfly eggs. Freshwat. Biol. 58:2287–98
    [Google Scholar]
  10. Bovill WD, Downes BJ, Lancaster J. 2015. Caddisfly egg mass morphology mediates egg predation: potential costs to individuals and populations. Freshwat. Biol. 60:360–72
    [Google Scholar]
  11. Brodin TF, Johansson F, Bergsten J. 2003. Predator related oviposition site selection of aquatic beetles (Hydroporus spp.) and effects on offspring life-history. Freshwat. Biol. 51:1277–85
    [Google Scholar]
  12. Bryant EH. 1969. A system favoring the evolution of holometabolous development. Ann. Entomol. Soc. Am. 62:1087–91
    [Google Scholar]
  13. Cain ML, Eccleston J, Kareiva PM. 1985. The influence of food plant dispersion on caterpillar searching success. Ecol. Entomol. 10:1–7
    [Google Scholar]
  14. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA. 1996. Recruitment and the local dynamics of open marine populations. Annu. Rev. Ecol. Syst. 27:477–500
    [Google Scholar]
  15. Center TD, Dray FA Jr. 2010. Bottom-up control of water hyacinth weevil populations: Do plants regulate insects?. J. Appl. Ecol. 47:329–37
    [Google Scholar]
  16. Clark CJ, Poulsen JR, Levey DJ, Osenberg CW. 2007. Are plant populations seed limited? A critique and meta-analysis of seed addition experiments. Am. Nat. 170:128–42
    [Google Scholar]
  17. Connolly SR, Menge BA, Roughgarden J. 2001. A latitudinal gradient in recruitment of intertidal invertebrates in the northeast Pacific Ocean. Ecology 82:1799–813
    [Google Scholar]
  18. Cornell HV, Hawkins BA. 1995. Survival patterns and mortality sources of herbivorous insects: some demographic trends. Am. Nat. 145:563–93
    [Google Scholar]
  19. Diaz-Paniagua C, Cespedes V, Andreu A, Lozano-Terol M, Keller C. 2019. Egg masses on the move: corixid oviposition on terrapin shells. Aquat. Insects 40:19–29
    [Google Scholar]
  20. Donnelly MA. 1989. Demographic effects of reproductive resource supplementation in a territorial frog, Dendrobates pumilio. Ecol. Monogr. 59:207–21
    [Google Scholar]
  21. Downes BJ, Lancaster J. 2010. Does dispersal control population densities in advection-dominated systems? A fresh look at critical assumptions and a direct test. J. Anim. Ecol. 79:235–48
    [Google Scholar]
  22. Downes BJ, Lancaster J. 2018. Itinerant, nomad or invader? A field experiment sheds light on the characteristics of successful dispersers and colonists. Freshwat. Biol. 63:1394–406
    [Google Scholar]
  23. Edgerly JS, Livdahl T. 1992. Density-dependent interactions within a complex life-cycle: the roles of cohort structure and mode of recruitment. J. Anim. Ecol. 61:139–50
    [Google Scholar]
  24. Ellis AM. 2008. Linking movement and oviposition behaviour to spatial population distribution in the tree hole mosquito Ochlerotatus triseriatus. J. Anim. Ecol. 77:156–66
    [Google Scholar]
  25. Encalada AC, Peckarsky BL. 2006. Selective oviposition behavior of the mayfly Baetis bicaudatus. Oecologia 148:526–37
    [Google Scholar]
  26. Encalada AC, Peckarsky BL. 2007. A comparative study of the costs of alternative mayfly oviposition behavior. Behav. Ecol. Sociobiol. 61:1437–48
    [Google Scholar]
  27. Encalada AC, Peckarsky BL. 2011. The influence of recruitment on within-generation population dynamics of a mayfly. Ecosphere 2:107
    [Google Scholar]
  28. Encalada AC, Peckarsky BL. 2012. Large-scale manipulation of mayfly recruitment affects population size. Oecologia 168:967–76
    [Google Scholar]
  29. Enders G, Wagner R. 1996. Mortality of Apatania fimbriata (Insecta: Trichoptera) during embryonic, larval and adult life stages. Freshwat. Biol. 36:93–104
    [Google Scholar]
  30. Faraji F, Janssen A, Sabelis MW. 2002. The benefits of clustering eggs: the role of egg predation and larval cannibalism in a predatory mite. Oecologia 131:20–26
    [Google Scholar]
  31. Floater GJ. 2001. Habitat complexity, spatial interference, and “Minimum Risk Distribution”: a framework for population stability. Ecol. Monogr. 71:447–68
    [Google Scholar]
  32. Fukumori H, Chee SY, Kano Y. 2013. Drilling predation on neritid egg capsules by the muricid snail Reishia clavigera. J. Molluscan Stud. 79:139–46
    [Google Scholar]
  33. Goldstein MC, Rosenberg M, Cheng L. 2012. Increased oceanic microplastic debris enhances oviposition in an endemic pelagic insect. Biol. Lett. 8:817–20
    [Google Scholar]
  34. Gould J, Clulow J, Clulow S. 2020. Food, not friend: Tadpoles of the sandpaper frog (Lechriodus fletcheri) cannibalise conspecific eggs as a food resource in ephemeral pools. Ethology 126:486–91
    [Google Scholar]
  35. Gunzburger MS, Travis J. 2005. Critical literature review of the evidence for unpalatability of amphibian eggs and larvae. J. Herpetol. 39:547–71
    [Google Scholar]
  36. Harabis R, Ruskova T, Dolny A. 2019. Different oviposition strategies of closely related damselfly species as an effective defense against parasitoids. Insects 10:26
    [Google Scholar]
  37. Harmon E, Allen J 2018. Predator-induced plasticity in egg capsule deposition in the mud snail Tritia obsoleta. Mar. Ecol. Prog. Ser. 586:113–25
    [Google Scholar]
  38. Heard SB. 1998. Resource patch density and larval aggregation in mushroom-breeding flies. Oikos 81:187–95
    [Google Scholar]
  39. Henrikson BI. 1990. Predation on amphibian eggs and tadpoles by common predators in acidified lakes. Ecography 13:201–6
    [Google Scholar]
  40. Heying HE. 2004. Reproductive limitation by oviposition site in a treehole breeding Madagascan poison frog (Mantella laevigata). Ecology and Evolution of Phytotelm-Breeding Anurans RM Lehtinen 23–30 Misc. Publ 193 Ann Arbor, MI: Mus. Zool., Univ. Mich.
    [Google Scholar]
  41. Hildrew AG, Woodward G, Winterbottom JH, Orton S 2004. Strong density dependence in a predatory insect: large-scale experiments in a stream. J. Anim. Ecol. 73:448–58
    [Google Scholar]
  42. Hixon MA, Pacala SW, Sandin SA. 2002. Population regulation: historical context and contemporary challenges of open versus closed systems. Ecology 83:1490–508
    [Google Scholar]
  43. Howard RD. 1978. Influence of male-defending oviposition sites on early embryo mortality in bullfrogs. Ecology 59:789–98
    [Google Scholar]
  44. Jaenike J. 1978. Optimal oviposition behavior in phytophagous insects. Theor. Popul. Biol. 14:350–56
    [Google Scholar]
  45. Karakas F, D'Oliveira D, Maas AE, Murphy DW 2018. Using a shell as a wing: pairing of dissimilar appendages in atlantiid heteropod swimming. J. Exp. Biol. 221:jeb192062
    [Google Scholar]
  46. Keough MJ, Downes BJ. 1982. Recruitment of marine invertebrates: the role of active larval choices and early mortality. Oecologia 54:348–52
    [Google Scholar]
  47. Khelifa R, Mellal MK. 2017. Host-plant-based restoration as a potential tool to improve conservation status of odonate specialists. Insect Conserv. Divers. 10:151–60
    [Google Scholar]
  48. Kilpatrick AM, Ives AR. 2003. Species interactions can explain Taylor's power law for ecological time series. Nature 422:65–68
    [Google Scholar]
  49. Kraus J, Vonesh J. 2012. Fluxes of terrestrial and aquatic carbon by emergent mosquitoes: a test of controls and implications for cross-ecosystem linkages. Oecologia 170:1111–22
    [Google Scholar]
  50. Kuhlmann M. 1994. Indirect effects of a predatory gastropod in a seagrass community. J. Exp. Mar. Biol. Ecol. 163:163–78
    [Google Scholar]
  51. Kuhlmann M. 1997. Regulation of fish reproduction by a predatory gastropod: an experimental investigation of indirect effects in a seagrass community. J. Exp. Mar. Biol. Ecol. 218:199–214
    [Google Scholar]
  52. Lancaster J, Belyea LR. 2006. Defining the limits to local density: alternative views of abundance–environment relationships. Freshwat. Biol. 51:783–96
    [Google Scholar]
  53. Lancaster J, Downes BJ. 2013. Aquatic Entomology Oxford, UK: Oxford Univ. Press
  54. Lancaster J, Downes BJ. 2014. Maternal behaviours may explain riffle-scale variations in some stream insect populations. Freshwat. Biol. 59:502–13
    [Google Scholar]
  55. Lancaster J, Downes BJ. 2017. Dispersal traits may reflect dispersal distances, but dispersers may not connect populations demographically. Oecologia 184:171–82
    [Google Scholar]
  56. Lancaster J, Downes BJ. 2018. Aquatic versus terrestrial insects: real or presumed differences in population dynamics?. Insects 9:157
    [Google Scholar]
  57. Lancaster J, Downes BJ, Arnold A 2010. Environmental constraints on oviposition limit egg supply of a stream insect at multiple scales. Oecologia 163:373–84
    [Google Scholar]
  58. Lancaster J, Downes BJ, Arnold A 2011. Lasting effects of maternal behaviour on the distribution of a dispersive stream insect. J. Anim. Ecol. 80:1061–69
    [Google Scholar]
  59. Lancaster J, Downes BJ, Dwyer G. 2020a. Terrestrial–aquatic transitions: Local abundances and movements of mature female caddisflies are related to oviposition habits but not flight capability. Freshwat. Biol. 65:908–19
    [Google Scholar]
  60. Lancaster J, Downes BJ, Lester RE, Rice SP. 2020b. Avoidance and aggregation create consistent egg distribution patterns of congeneric caddisflies across spatially variable oviposition landscapes. Oecologia 192:375–89
    [Google Scholar]
  61. Lancaster J, Downes BJ, Reich P. 2003. Linking landscape patterns of resource distribution with models of aggregation in ovipositing stream insects. J. Anim. Ecol. 72:969–78
    [Google Scholar]
  62. Macqueen A. 2015. Implications of oviposition site selection and habitat limitation for caddisfly populations in sand-bed streams. PhD thesis University of Melbourne Melbourne, Australia:
    [Google Scholar]
  63. Macqueen A, Downes BJ. 2015. Large-scale manipulation of oviposition substrata affects egg supply to populations of some stream-dwelling caddisflies. Freshwat. Biol. 60:802–12
    [Google Scholar]
  64. Mayhew PJ. 2001. Herbivore host choice and optimal bad motherhood. Trends Ecol. Evol. 16:165–67
    [Google Scholar]
  65. Menge BA, Chan F, Dudas S, Eerkes-Medrano D, Grorud-Colvert K et al. 2009. Terrestrial ecologists ignore aquatic literature: asymmetry in citation breadth in ecological publications and implications for generality and progress in ecology. J. Exp. Mar. Biol. Ecol. 377:93–100
    [Google Scholar]
  66. Murdoch WW. 1994. Population regulation in theory and practice. Ecology 75:271–87
    [Google Scholar]
  67. Ode P. 2002. The role of competition in the foraging ecology of two herbivorous stream mayflies. PhD thesis Cornell University Ithaca, NY:
    [Google Scholar]
  68. Peckarsky BL, Allan JD, McIntosh AR, Taylor BW 2010. Understanding the role of predation in open systems: the value of place-based research. The Ecology of Place I Billick, MV Price 185–206 Chicago, IL: Univ. Chicago Press
    [Google Scholar]
  69. Peckarsky BL, Taylor BW, Caudill CC. 2000. Hydrologic and behavioral constraints on oviposition in stream insects: implications for adult dispersal. Oecologia 125:186–200
    [Google Scholar]
  70. Petranka JW, Hopey ME, Jennings BT, Baird SD, Boone SJ. 1994. Breeding habitat segregation of wood frogs and American toads: the role of interspecific tadpole predation and adult choice. Copeia 1994:691–97
    [Google Scholar]
  71. Poulsen JR, Osenberg CW, Clark CJ, Levey DJ, Bolker BM. 2007. Plants as reef fish: fitting the functional form of seedling recruitment. Am. Nat. 170:167–83
    [Google Scholar]
  72. Power ME, Dietrich WE, Sullivan KO 1998. Experimentation, observation, and inference in river and watershed investigations. Experimental Ecology: Issues and Perspectives WJ Resetarits Jr., J Bernardo 113–32 New York, NY: Oxford Univ. Press
    [Google Scholar]
  73. Price PW, Craig TP, Hunter MD 1998. Population ecology of a gall-inducing sawfly, Euura lasiolepis, and relatives. Insect Populations JP Dempster, IFG McLean 324–40 Dordrecht, Holland: Kluwer Acad. Publ.
    [Google Scholar]
  74. Pulliam HR, Waser NM 2010. Ecological invariance and the search for generality in ecology. The Ecology of Place I Billick, MV Price 69–92 Chicago, IL: Univ. Chicago Press
    [Google Scholar]
  75. Purcell AH, Hoffmann A, Resh VH. 2008. Life history of a dipteran predator (Scathophagidae: Acanthocnema) of insect egg masses in a northern California stream. Freshwat. Biol. 53:2426–37
    [Google Scholar]
  76. Rausher MD. 1979. Larval habitat suitability and oviposition preference in three related butterflies. Ecology 60:503–11
    [Google Scholar]
  77. Refsnider JM, Janzen FJ. 2010. Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu. Rev. Ecol. Evol. Syst. 41:39–57
    [Google Scholar]
  78. Reich P, Downes BJ. 2003a. The distribution of aquatic invertebrate egg masses in relation to the physical characteristics of oviposition sites at two Victorian upland streams. Freshwat. Biol. 48:1497–513
    [Google Scholar]
  79. Reich P, Downes BJ. 2003b. Experimental evidence for physical cues involved in oviposition site selection of lotic hydrobiosid caddis flies. Oecologia 136:465–75
    [Google Scholar]
  80. Reich P, Downes BJ. 2004. Relating larval distributions to patterns of oviposition: evidence from lotic hydrobiosid caddisflies. Freshwat. Biol. 49:1423–36
    [Google Scholar]
  81. Reich P, Hale R, Downes BJ, Lancaster J. 2011. Environmental cues or conspecific attraction as causes for egg mass aggregation in hydrobiosid caddisflies. Hydrobiologia 661:351–62
    [Google Scholar]
  82. Resetarits WJ. 2001. Colonization under threat of predation: avoidance of fish by an aquatic beetle, Tropisternus lateralis (Coleoptera: Hydrophilidae). Oecologia 129:155–60
    [Google Scholar]
  83. Rodrigues M, de Oliveira Roque F, Guillermo-Ferreira R, Saito V, Samways M 2019. Egg-laying traits reflect shifts in dragonfly assemblages in response to different amount of tropical forest cover. Insect Conserv. Divers. 12:231–40
    [Google Scholar]
  84. Rouquette JR, Thompson DJ. 2007. Patterns of movement and dispersal in an endangered damselfly and the consequences for its management. J. Appl. Ecol. 44:692–701
    [Google Scholar]
  85. Schiel DR. 2004. The structure and replenishment of rocky shore intertidal communities and biogeographic comparisons. J. Exp. Mar. Biol. Ecol. 300:309–42
    [Google Scholar]
  86. Schiers J, De Bruyn L, Verhagen R. 2000. Optimization of adult performance determines host choice in a grass miner. Proc. R. Soc. B 267:2065–69
    [Google Scholar]
  87. Schmitt RJ, Holbrook SJ. 2000. Habitat-limited recruitment of coral reef damselfish. Ecology 81:3479–94
    [Google Scholar]
  88. Schmitt RJ, Holbrook SJ, Osenberg CW. 1999. Quantifying the effects of multiple processes on local abundance: a cohort approach for open populations. Ecol. Lett. 2:294–303
    [Google Scholar]
  89. Smith C, Reynolds J, Sutherland J, Juraida P. 2000a. Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav. Ecol. Sociobiol. 48:29–35
    [Google Scholar]
  90. Smith C, Reynolds J, Sutherland W. 2000b. Population consequences of reproductive decisions. Proc. R. Soc. B 267:1327–34
    [Google Scholar]
  91. Smith R. 1976. Brooding behaviour of male water bug Belostoma flumineum (Hemiptera: Belostomatidae). J. Kans. Entomol. Soc. 49:333–43
    [Google Scholar]
  92. Smith RF, Alexander LC, Lamp WO. 2009. Dispersal by terrestrial stages of stream insects in urban watersheds: a synthesis of current knowledge. J. N. Am. Benthol. Soc. 28:1022–37
    [Google Scholar]
  93. Solbreck C, Ives AR. 2007. Density dependence versus independence, and irregular population dynamics of a swallow-wort fruit fly. Ecology 88:1466–75
    [Google Scholar]
  94. Spencer M, Blaustein L, Cohen JE. 2002. Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83:669–79
    [Google Scholar]
  95. Spight TM. 1977. Do intertidal snails spawn in the right places?. Evolution 31:682–91
    [Google Scholar]
  96. Stiling PD. 1987. The frequency of density dependence in insect host-parasitoid systems. Ecology 68:844–56
    [Google Scholar]
  97. Strauss T, Kulkarni D, Preuss T, Hammers-Wirtz M. 2016. The secret lives of cannibals: modelling density-dependent processes that regulate population dynamics in Chaoborus crystallinus. Ecol. Model. 321:84–97
    [Google Scholar]
  98. Strong D, Lawton J, Southwood R 1984. Insects on Plants: Community Patterns and Mechanisms Cambridge, MA: Harvard University Press
  99. Swanson CA. 2004. Effect of substrate availability and conspecific cues on communal oviposition in the apple murex snail Phyllonotus pomum. Mar. Ecol. Prog. Ser. 275:175–84
    [Google Scholar]
  100. Thompson JN, Pellmyr O. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annu. Rev. Entomol. 36:65–89
    [Google Scholar]
  101. von Dassow Y, Strathmann RR. 2005. Full of eggs and no place to lay them: hidden cost of benthic development. Mar. Ecol. Prog. Ser. 294:23–34
    [Google Scholar]
  102. Waldman BD. 1982. Adaptive significance of communal oviposition in wood frogs (Rana sylvatica). Behav. Ecol. Sociobiol. 10:169–74
    [Google Scholar]
  103. Werner EE 1988. Size, scaling and the evolution of complex life cycles. Size-Structured Populations B Ebenman, L Persson 60–81 Berlin: Springer-Verlag
    [Google Scholar]
  104. Wilbur HM. 1980. Complex life cycles. Annu. Rev. Ecol. Syst. 11:67–93
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-122420-102909
Loading
/content/journals/10.1146/annurev-ecolsys-122420-102909
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error