Plasticity in extended phenotypes: how the antlion Myrmeleon crudelis adjusts the pit traps depending on biotic and abiotic conditions

In: Israel Journal of Ecology and Evolution
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  • a LIHO (Laboratorio de Investigaciones en Hormigas), INIBIOMA, CONICET and CRUB-Universidad Nacional del Comahue, Argentina
  • | b STRI (Smithsonian Tropical Research Institute), Panamá

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Abstract

The physical structures built by animals are considered extended phenotypes that reflect how organisms make decisions and deal with changes in their biotic and abiotic environment. We summarize the results of several studies on Myrmeleon crudelis, a neuropteran larva that digs pit-traps in the soil to capture small arthropods (mostly ants) in the tropical dry forests of Costa Rica. Specifically, we showed how this species responds to varying biotic and abiotic conditions with changes in the design and/or location of its pit traps. Several experiments and field comparisons indicate that: 1) antlions adjust the pit design according to the abundance and type of prey. When prey is scarce, antlions increased trap diameter, an architectural adjustment that enhances the probability of prey encounter. Antlions that experienced high prey abundance, but the prey easily escaped, then increased pit depth, an adjustment that increases the chance of prey retention; 2) soil compaction strongly reduced pit-trap size and abundance; 3) antlions preferred soils with high proportion of fine-particle size to build pits. In fine-grained soil, pit-traps are larger and more efficient to capture prey than traps in coarse-grained soils; and 4) pit-traps may also be affected through indirect effects of soil structure and vegetation cover. Areas with fine-soil presented less plant cover, and plant cover could be beneficial for antlions because it acts as a shelter against direct sunlight and rainfall, or it may represent a cost because it is a source of leaflitter falling in the pits. The works summarized here how trap-building predators can exhibit considerable flexibility in trap construction in response to various biotic and abiotic factors, emphasizing how the study of extended phenotypes can be a useful approach to better understand the flexibility of foraging behaviors.

  • Adar S. , Dor R. (2018). Mother doesn’t always know best: Maternal wormlion choice of oviposition habitat does not match larval habitat choice. Behavioural Processes 147: 1-4.

    • Search Google Scholar
    • Export Citation
  • Adar S. , Dor R. , Scharf I. (2016). Habitat choice and complex decision making in a trap-building predator. Behavioral Ecology 27: 14911498.

    • Search Google Scholar
    • Export Citation
  • Amador-Vargas S. (2012). Plant killing by mutualistic ants increases the density of host species seedlings in the dry forest of Costa Rica. Psyche: A Journal of Entomology 2012: 16. DOI:10.1155/2012/491592

    • Search Google Scholar
    • Export Citation
  • Bar-Ziv M.A. , Bega D. , Subach A. , Scharf I. (2018). Wormlions prefer both fine and deep sand but only deep sand leads to better performance. Current Zoology: zoy065.

    • Search Google Scholar
    • Export Citation
  • Benvenuti B. , Walsh J. , O’Brien K. M. , Kovach A.I. (2018). Plasticity in nesting adaptations of a tidal marsh endemic bird. Ecology and Evolution ,8: 1078010793.

    • Search Google Scholar
    • Export Citation
  • Blamires S. J. (2010). Plasticity in extended phenotypes: orb web architectural responses to variations in prey parameters. Journal of Experimental Biology, 213: 32073212.

    • Search Google Scholar
    • Export Citation
  • Botz J.T. , Loudon C. , Barger J.B. , Olafsen J.S. , Steeples D.W. (2003). Effects of slope and particle size on ant locomotion: implications for choice of substrate by antlions. J. Kansas Entomol. Soc. 76: 426435.

    • Search Google Scholar
    • Export Citation
  • Crowley P.H. , Linton M.C. (1999). Antlion foraging: tracking prey across space and time. Ecology, 80(7): 22712282.

  • Dawkins R. (1982). The Extended Phenotype. Oxford, UK: Oxford University Press. 287 pp.

  • Devetak D. , Špernjak A. , Janžekovic F. (2005). Substrate particle size affects pit building decision and pit size in the antlion larvae Euroleon nostras (Neuroptera: Myrmeleontidae). Physiological Entomology, 30(2): 158163.

    • Search Google Scholar
    • Export Citation
  • Devetak D. (2008). Substrate particle size-preference of wormlion Vermileo vermileo (Diptera: Vermileonidae) larvae and their interaction with antlions. Eur. J. Entomol. 105: 631635

    • Search Google Scholar
    • Export Citation
  • Devetak D. , Arnett A.E. (2015). Preference of antlion and wormlion larvae (Neuroptera: Myrmeleontidae; Diptera: Vermileonidae) for substrates according to substrate particle sizes. Eur. J. Entomol., 112: 500509.

    • Search Google Scholar
    • Export Citation
  • Eisner T. , Nowicki S. (1983). Spider web protection through visual advertisement: role of the stabilimentum. Science, 219: 185187.

  • Elimelech E. , Pinshow B. (2008). Variation in food availability influences prey-capture method in antlion larvae. Ecological Entomology, 33: 652662.

    • Search Google Scholar
    • Export Citation
  • Farji-Brener A.G. (2003). Microhabitat selection by antlion larvae, Myrmeleon crudelis: effect of soil particle size on pit-trap design and prey capture. Journal of Insect Behavior, 16: 783796.

    • Search Google Scholar
    • Export Citation
  • Farji-Brener A.G. , Carvajal D. , Gei M.G. , Olano J. , Sanchez J.D. (2008). Direct and indirect effects of soil structure on the density of an antlion larva in a tropical dry forest. Ecological Entomology, 33: 183188.

    • Search Google Scholar
    • Export Citation
  • Farji-Brener A.G. , Chinchilla F. , Umaña M.N. , Ocasio-Torres M.E. , Chauta-Mellizo A. , Acosta-Rojas D. , Marinaro F. , De Torres Curth M. , Amador-Vargas S. (2015). Branching angles reflect a trade-off between reducing trail maintenance costs or travel distances in leaf-cutting ants. Ecology, 96(2): 510517.

    • Search Google Scholar
    • Export Citation
  • Fertin A. , Casas J. (2006). Efficiency of antlion trap construction. Journal of Experimental Biology, 209: 35103515.

  • Franks N.R. , Worley A. , Falkenberg M. , Sendova-Franks A.B. , Christensen K. (2019). Digging the optimum pit: antlions, spirals and spontaneous stratification. Proceedings of the Royal Society B, 286: 20190365.

    • Search Google Scholar
    • Export Citation
  • Gatti M.G. and Farji-Brener A.G. (2002). Low density of ant lion larva (Myrmeleon crudelis) in ant-acacia clearings: high predation risk or inadequate substrate? Biotropica, 34: 458462.

    • Search Google Scholar
    • Export Citation
  • Gotelli N.J. (1993). Ant lion zones: causes of high density predator aggregations. Ecology, 74: 226237.

  • Gotelli N.J. (1996). Ant community structure: effects of predatory ant lions. Ecology, 77(2): 630638.

  • Gotelli N.J. (1997). Competition and coexistence of larval ant lions. Ecology, 78(6): 17611773.

  • Griffiths D. (1980). The feeding biology of ant-lion larvae: prey capture, handling and utilization. The Journal of Animal Ecology 49: 99125.

    • Search Google Scholar
    • Export Citation
  • Griffiths D. (1986). Pit construction by ant-lion larvae: a cost-benefit analysis. The Journal of Animal Ecology, 55: 3957.

  • Hansell M.H. (2005). Animal Architecture. Oxford, UK: Oxford University Press. 313 pp.

  • Hesselberg T. (2015). Exploration behavior and behavioral flexibility in orb-web spiders: a review. Current Zoology, 61: 313327.

  • Heinrich B. , Heinrich M.J. (1984). The pit-trapping foraging strategy of the ant lion, Myrmeleon immaculatus DeGeer (Neuroptera: Myrmeleontidae). Behavioral Ecology and Sociobiology, 14(2): 151160.

    • Search Google Scholar
    • Export Citation
  • Hölldobler B. , Wilson E.O. (1990). The Ants. Harvard University Press. 732 pp.

  • Hollis K.L. , Cogswell H. , Snyder K. , Guillette L.M. , Nowbahari E. (2011). Specialized learning in antlions (Neuroptera: Myrmeleontidae), pit-digging predators, shortens vulnerable larval stage. PLOS ONE 6: . DOI:10.1371/journal.pone.0017958

    • Search Google Scholar
    • Export Citation
  • Jaffé R. , Eberhard W. , De Angelo C. , Eusse D. , Gutierrez A. , Quijas S. , Rodriguez A ,. Rodríguez M. (2006). Caution, webs in the way! Possible functions of silk stabilimenta in Gasteracantha cancriformis (Araneae, Araneidae). Journal of Arachnology, 34: 448455.

    • Search Google Scholar
    • Export Citation
  • Kaspari M. , Weiser M.D. (1999). The size–grain hypothesis and interspecific scaling in ants. Functional Ecology, 13: 530538.

  • Klokočovnik V. , Devetak D. , Orlačnik M. (2012). Behavioral plasticity and variation in pit construction of antlion larvae in substrates with different particle sizes. Ethology, 118: 11021110.

    • Search Google Scholar
    • Export Citation
  • Loiterton S.J. , Magrath R.D. (1996). Substrate type affects partial prey consumption by larvae of the antlion Myrmeleon acer (Neuroptera: myrmeleontidae). Aust. J. Zool., 44: 589597.

    • Search Google Scholar
    • Export Citation
  • Lomascolo S. , Farji-Brener A.G. (2001). Adaptive short-term changes in pit design by antlion larvae (Myrmeleon sp.) in response to different prey conditions. Ethology Ecology and Evolution, 13: 393397.

    • Search Google Scholar
    • Export Citation
  • Lucas J.R. (1982). The biophysics of pit construction by antlion larvae (Myrmeleon, Neuroptera). Animal Behavior, 30: 651664.

  • Lucas J.R. (1985). Metabolic rates and pit-construction costs of two antlion species. The Journal of Animal Ecology, 54: 295309.

  • Lucas J.R. , Brockmann H.J. (1981). Predatory interactions between ants and antlions (Hymenoptera: Formicidae and Neuroptera: Myrmeleontidae). Journal of the Kansas Entomological Society, 54(2): 228232.

    • Search Google Scholar
    • Export Citation
  • Mainwaring M.C. , Hartley I.R. , Bearhop S. , Brulez K. , du Feu C.R. , Murphy G. , Plummer K. , Webber S. , Reynolds S. , Deeming D.C. (2012). Latitudinal variation in blue tit and great tit nest characteristics indicates environmental adjustment. Journal of Biogeography, 39: 16691677.

    • Search Google Scholar
    • Export Citation
  • Matsura T. , Yamaga Y. , Itoh M. (2005). Substrate selection for pit making and oviposition in an antlion, Myrmeleon bore Tjeder, in terms of sand particle size. Entomological Science, 8: 347353.

    • Search Google Scholar
    • Export Citation
  • McClure M.S. (1976). Spatial distribution of pit-making ant lion larvae (Neuroptera: Myrmeleontidae): density effects. Biotropica, 8(3): 179183.

    • Search Google Scholar
    • Export Citation
  • Miler K. , Yahya B.E. , Czarnoleski M. (2018). Different predation efficiencies of trap-building larvae of sympatric antlions and wormlions from the rainforest of Borneo. Ecological entomology, 43(2): 255262.

    • Search Google Scholar
    • Export Citation
  • Morrison L.W. (2004). Spatiotemporal variation in antlion (Neuroptera: Myrmeleontidae) density and impacts on ant (Hymenoptera: Formicidae) and generalized arthropod foraging. Annals of the Entomological Society of America, 97(5): 913922.

    • Search Google Scholar
    • Export Citation
  • Pyke G.H. , Pulliam H. , Charnov E. (1977). Optimal foraging: a selective review of theory and tests. Quarterly Review of Biology, 52: 137154.

    • Search Google Scholar
    • Export Citation
  • Scharf I. , Ovadia O. (2006). Factors influencing site abandonment and site selection in a sit-and-wait predator: a review of pit-building antlion larvae. Journal of Insect Behavior, 19: 197218.

    • Search Google Scholar
    • Export Citation
  • Scharf I. , Golan B. , Ovadia O. (2009). The effect of sand depth, feeding regime, density, and body mass on the foraging behaviour of a pit-building antlion. Ecological Entomology, 34: 2633.

    • Search Google Scholar
    • Export Citation
  • Scharf I. , Barkae E.D. , Ovadia O. (2010). Response of pit-building antlions to repeated unsuccessful encounters with prey. Animal behavior, 79: 153158.

    • Search Google Scholar
    • Export Citation
  • Scharf I. , Lubin Y. , Ovadia O. (2011). Foraging decisions and behavioural flexibility in trap-building predators: a review. Biological Reviews, 86: 626639.

    • Search Google Scholar
    • Export Citation
  • Turner J.S. (2009). The Extended Organism: The Physiology of Animal-Built Structures. Harvard University Press. 235 pp.

  • Wilson D.S. (1974). Prey capture and competition in the ant lion. Biotropica, 6(3): 187193.

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