Consequences of envenomation: red imported fire ants have delayed effects on survival but not growth of native fence lizards
Tracy Langkilde A B and Nicole A. Freidenfelds A
+ Author Affiliations
- Author Affiliations
A 208 Mueller Lab, The Pennsylvania State University, University Park, PA 16802, USA.
B Corresponding author. Email: tll30@psu.edu
Wildlife Research 37(7) 566-573 https://doi.org/10.1071/WR10098
Submitted: 18 June 2010 Accepted: 2 October 2010 Published: 17 December 2010
Abstract
Context: Aggressive encounters, including those with venomous species, impose selective pressure on native species. Immediate lethal outcomes of these encounters have been the primary focus of research in this field. However, not all aggressive interactions result in immediate mortality, and indirect consequences of aggressive interactions may be an equally important but under-considered selective force. The red imported fire ant is a globally important venomous invader that imposes novel selective pressure on native communities.
Aims: We examined indirect effects of fire ant envenomation on native fence lizard growth rates and subsequent survival.
Methods: Fence lizards are subject to fire ant envenomation in the field when they eat fire ants (they are stung inside the mouth) and through fire ant attack (they are stung on the body). We quantified body sizes of adult lizards from fire ant-invaded and uninvaded sites. We then experimentally exposed hatchling fence lizards to the two modes of fire ant envenomation, and quantified their growth and survival over 1 year.
Key results: Lizards from fire ant-invaded sites were smaller than those from an uninvaded site, even at similar latitudes. However, in contrast to studies on other native taxa, we found no effect of fire ant venom on growth rates of lizards from naïve or fire ant-invaded populations. Lizards exposed to fire ant venom, through both eating and attack, experienced higher rates of delayed mortality, with 34% of lizards dying 1–11 weeks post-envenomation compared with 12% of lizards in the control treatment. These patterns were true for fire ant naïve populations as well as those exposed to fire ants for ~35 generations.
Conclusions: These results suggest that the smaller body sizes observed in fence lizards from fire ant-invaded sites are not a consequence of exposure to fire ant venom. However, fence lizards from both sites suffer delayed survival costs of fire ant envenomation.
Implications: The present study highlights the importance of considering indirect fitness consequences of aggressive encounters if we are to fully understand the ecological and evolutionary consequences of these interactions, and adequately manage and predict the impacts of invasive species.
References
Abrams, P. A., and Rowe, L. (1996). The effects of predation on the age and size of maturity of prey. Evolution 50, 1052–1061.| The effects of predation on the age and size of maturity of prey.Crossref | GoogleScholarGoogle Scholar |
Allen, C. R., Rice, K. G., Wojcik, D. P., and Percival, H. F. (1997). Effect of red imported fire ant envenomization on neonatal American alligators. Journal of Herpetology 31, 318–321.
| Effect of red imported fire ant envenomization on neonatal American alligators.Crossref | GoogleScholarGoogle Scholar |
Allen, C. R., Forys, E. A., Rice, K. G., and Wojcik, D. P. (2001). Effects of fire ants (Hymenoptera: Formicidae) on hatching turtles and prevalence of fire ants on sea turtle nesting beaches in Florida. The Florida Entomologist 84, 250–253.
| Effects of fire ants (Hymenoptera: Formicidae) on hatching turtles and prevalence of fire ants on sea turtle nesting beaches in Florida.Crossref | GoogleScholarGoogle Scholar |
Allen, C. R., Epperson, D. M., and Garmestani, A. S. (2004). Red imported fire ant impacts on wildlife: a decade of research. American Midland Naturalist 152, 88–103.
| Red imported fire ant impacts on wildlife: a decade of research.Crossref | GoogleScholarGoogle Scholar |
Angilletta, M. J. J., Niewiarowski, P. H., Dunham, A. E., Leaché, A. D., and Porter, W. P. (2004). Bergmann’s clines in ectotherms: illustrating a life-history perspective with Sceloporine lizards. American Naturalist 164, E168–E183.
| Bergmann’s clines in ectotherms: illustrating a life-history perspective with Sceloporine lizards.Crossref | GoogleScholarGoogle Scholar |
Berven, K. A., and Boltz, R. S. (2001). Interactive effects of leech (Desserobdella picta) infection on wood frog (Rana sylvatica) tadpole fitness traits. Copeia 2001, 907–915.
| Interactive effects of leech (Desserobdella picta) infection on wood frog (Rana sylvatica) tadpole fitness traits.Crossref | GoogleScholarGoogle Scholar |
Biardi, J. E., Coss, R. G., and Smith, D. G. (2000). California ground squirrel (Spermophilus beecheyi) blood sera inhibits crotalid venom proteolytic activity. Toxicon 38, 713–721.
| California ground squirrel (Spermophilus beecheyi) blood sera inhibits crotalid venom proteolytic activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXot1WrtA%3D%3D&md5=65f499befa64c852425947a7943b3ce0CAS | 10673162PubMed |
Blum, M. S., Walker, J. R., Callahan, P. S., and Novak, A. F. (1958). Chemical, insecticidal, and antibiotic properties of fire ant venom. Science 128, 306–307.
| Chemical, insecticidal, and antibiotic properties of fire ant venom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1cXptlagtg%3D%3D&md5=7517dca466b2c3682613b932536deb6cCAS |
Bøhn, T., Sandlund, O. T., Amundsen, P., and Primicerio, R. (2004). Rapidly changing life history during invasion. Oikos 106, 138–150.
| Rapidly changing life history during invasion.Crossref | GoogleScholarGoogle Scholar |
Boronow, K., and Langkilde, T. (2010). Sublethal effects of invasive fire ant venom on a native lizard. Journal of Experimental Zoology Part A 313A, 17–23.
| Sublethal effects of invasive fire ant venom on a native lizard.Crossref | GoogleScholarGoogle Scholar |
Bull, C. M., Burzacott, D., and Sharrad, R. D. (1989). No competition for resources between two tick species at their parapatric boundary. Oecologia 79, 558–562.
| No competition for resources between two tick species at their parapatric boundary.Crossref | GoogleScholarGoogle Scholar |
Callcott, A. A., and Collins, H. L. (1996). Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918–1995. The Florida Entomologist 79, 240–251.
| Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918–1995.Crossref | GoogleScholarGoogle Scholar |
Code of Federal Regulations (2010). ‘Title 7. Part 301.81. Subpart – Imported Fire Ant.’ Available at http://ecfr.gpoaccess.gov [accessed 15 February 2010].
Conant, R., and Collins, J. T. (1998). ‘A Field Guide to Reptiles and Amphibians of Eastern and Central North America.’ 3rd edn. (Houghton Mifflin Company: Boston, MA.)
Fell, P. E., and Balsamo, A. M. (1985). Recruitment of Mytilus edulis L. in the Thames Estuary, with evidence for differences in the time of maximal settling along the Connecticut shore. Estuaries 8, 68–75.
Ferguson, G. W., and Fox, S. F. (1984). Annual variation of survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 38, 342–349.
| Annual variation of survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance.Crossref | GoogleScholarGoogle Scholar |
Ferguson, G. W., and Talent, L. G. (1993). Life-history traits of the common lizard Sceloporus undulatus from two populations raised in a common laboratory environment. Oecologia 93, 88–94.
Fox, S. F., and McCoy, J. K. (2000). The effects of tail loss on survival, growth, reproduction, and sex ratio of offspring in the lizard Uta stansburiana in the field. Oecologia 122, 327–334.
| The effects of tail loss on survival, growth, reproduction, and sex ratio of offspring in the lizard Uta stansburiana in the field.Crossref | GoogleScholarGoogle Scholar |
Freeman, A. S., and Byers, J. E. (2006). Divergent induced responses to an invasive predator in marine mussel populations. Science 313, 831–833.
| 1:CAS:528:DC%2BD28XnvVynt74%3D&md5=6c2589107f672424d7a03961f9d98465CAS | 16902136PubMed |
Fritzen, M., Schattner, M., Quintana Ribeiro, A. L., de Fátima Correia Batista, I., Ventura, J., Prezoto, B. C., and Chudzinski-Tavassi, A. M. (2003). Lonomia obliqua venom action on fibrinolytic system. Thrombosis Research 112, 105–110.
| Lonomia obliqua venom action on fibrinolytic system.Crossref | GoogleScholarGoogle Scholar | 15013281PubMed |
Gadgil, M., and Bossert, W. H. (1970). Life historical consequences of natural selection. American Naturalist 104, 1–24.
| Life historical consequences of natural selection.Crossref | GoogleScholarGoogle Scholar |
Giuliano, W. M., Allen, C. R., Lutz, R. S., and Demarais, S. (1996). Effects of red imported fire ants on northern bobwhite chicks. The Journal of Wildlife Management 60, 309–313.
| Effects of red imported fire ants on northern bobwhite chicks.Crossref | GoogleScholarGoogle Scholar |
Gotelli, N. J., and Arnett, A. E. (2000). Biogeographic effects of red fire ant invasion. Ecology Letters 3, 257–261.
| Biogeographic effects of red fire ant invasion.Crossref | GoogleScholarGoogle Scholar |
Haenel, G. J., and John-Alder, H. B. (2002). Experimental and demographic analyses of growth rate and sexual size dimorphism in a lizard, Sceloporus undulatus. Oikos 96, 70–81.
| Experimental and demographic analyses of growth rate and sexual size dimorphism in a lizard, Sceloporus undulatus.Crossref | GoogleScholarGoogle Scholar |
Haight, K. L., and Tschinkel, W. R. (2003). Patterns of venom synthesis and use in the fire ant, Solenopsis invicta. Toxicon 42, 673–682.
| Patterns of venom synthesis and use in the fire ant, Solenopsis invicta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosFOrs7w%3D&md5=602c69ece8c5c9b49c56f624014d30e9CAS | 14602123PubMed |
Holtcamp, W. N., Grant, W. E., and Vinson, S. B. (1997). Patch use under predation hazard: effect of the red imported fire ant on deer mouse foraging behavior. Ecology 78, 308–317.
| Patch use under predation hazard: effect of the red imported fire ant on deer mouse foraging behavior.Crossref | GoogleScholarGoogle Scholar |
Howell, G., Butler, J., deShazo, R. D., Farley, J. M., Liu, H.-L., Nanayakkara, N. P. D., Yates, A., Yi, G. B., and Rockhold, R. W. (2005). Cardiodepressant and neurologic actions of Solenopsis invicta (imported fire ant) venom alkaloids. Annals of Allergy, Asthma & Immunology 94, 380–386.
| Cardiodepressant and neurologic actions of Solenopsis invicta (imported fire ant) venom alkaloids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Wgu7s%3D&md5=04794744504c372b617a689483cea113CAS |
Hutchings, J. A. (1993). Adaptive life histories effected by age-specific survival and growth rate. Ecology 74, 673–684.
| Adaptive life histories effected by age-specific survival and growth rate.Crossref | GoogleScholarGoogle Scholar |
Hutton, R. A., and Warrell, D. A. (1993). Action of snake venom components on the haemostatic system. Blood Reviews 7, 176–189.
| Action of snake venom components on the haemostatic system.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FmtVOltg%3D%3D&md5=bec4141da62bc75089070917f0bd318fCAS | 8241832PubMed |
Johnson, P. T. J., Preu, E. R., Sutherland, D. R., Romansic, J. M., Han, B., and Blaustein, A. R. (2006). Adding infection to injury: synergistic effects of predation and parasitism on amphibian malformations. Ecology 87, 2227–2235.
| Adding infection to injury: synergistic effects of predation and parasitism on amphibian malformations.Crossref | GoogleScholarGoogle Scholar | 16995623PubMed |
Kardong, K. V. (1982). The evolution of the venom apparatus in snakes from colubrids to viperids and elapids. Memorias do Instituto Butantan 46, 105–118.
Krahe, H. (2005). ‘Impact of the Red Imported Fire Ant (Solenopsis invicta) on Two Species of Sea Turtle Hatchlings.’ (Florida Atlantic University: Boca Raton, FL.)
Langerhans, R. B. (2007). Evolutionary consequences of predation: avoidance, escape, reproduction, and diversification. In ‘Predation in Organisms: a Distinct Phenomenon’. (Ed. A. M. T. Elewa.) pp. 177–220. (Springer-Verlag: Berlin.)
Langkilde, T. (2009). Invasive fire ants alter behavior and morphology of native lizards. Ecology 90, 208–217.
| Invasive fire ants alter behavior and morphology of native lizards.Crossref | GoogleScholarGoogle Scholar | 19294926PubMed |
Laurie, A. W. (1989) Effects of the 1982–83 El Nino–southern oscillation event on marine iguana (Amblyrhynchus cristatus Bell, 1825) populations in the Galapagos. In ‘Global Ecological Consequences of the 1982–83 El Nino–Southern Oscillation’. (Ed. P. W. Glynn.) pp. 361–380. (Elsevier: New York.)
Lawrence, J. M., and Vasquez, J. (1996). The effect of sublethal predation on the biology of echinoderms. Oceanologica Acta 19, 431–440.
Lewis, R. L., and Gutmann, L. (2004). Snake venoms and the neuromuscular junction. Seminars in Neurology 24, 175–179.
| Snake venoms and the neuromuscular junction.Crossref | GoogleScholarGoogle Scholar | 15257514PubMed |
Lima, S. L. (1998). Nonlethal effects in the ecology of predator–prey interactions. Bioscience 48, 25–34.
| Nonlethal effects in the ecology of predator–prey interactions.Crossref | GoogleScholarGoogle Scholar |
MacConnell, J. G., Blum, M. S., and Fales, H. M. (1971). The chemistry of fire ant venom. Tetrahedron 27, 1129–1139.
| The chemistry of fire ant venom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXktVentb4%3D&md5=04614f456e152a04772c5a7f499cbb33CAS |
Maynard Smith, J. M., Harper, D. G. C., and Brookfield, J. F. Y. (1988). The evolution of aggression: can selection generate variability? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 319, 557–570.
| The evolution of aggression: can selection generate variability?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FpvFehtw%3D%3D&md5=14455baacf0ea15ef1eb2defc12367a6CAS | 2905492PubMed |
Montgomery, W. B. (1996). Predation by the fire ant, Solenopsis invicta, on the three-toed box turtle, Terrapene carolina triunguis. Bulletin of the Chicago Herpetological Society 31, 105–106.
Mooney, H. A., and Cleland, E. E. (2001). The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences, USA 98, 5446–5451.
| The evolutionary impact of invasive species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Wgurw%3D&md5=02690ea111a25b5eeed78785c9e8477dCAS |
Olivera, B. M. (1999). Conus venom peptides: correlating chemistry and behavior. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 185, 353–359.
| Conus venom peptides: correlating chemistry and behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotVCjs7w%3D&md5=8404d95d03442ff2b87f06c98a8a633cCAS |
Omran, M. A. A., Abdel-Rahman, M. S., and Nabil, Z. I. (1992). Effect of scorpion Leiurus quinquestriatus (H&E) venom on rat’s heart rate and blood pressure. Toxicology Letters 61, 111.
| Effect of scorpion Leiurus quinquestriatus (H&E) venom on rat’s heart rate and blood pressure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XkvVCqt7Y%3D&md5=96c060b6c0beff4d1dfe4e32b772ca63CAS | 1609434PubMed |
Parker, W. S. (1994). Demography of the fence lizard, Sceloporus undulatus, in northern Mississippi. Copeia 1994, 136–152.
| Demography of the fence lizard, Sceloporus undulatus, in northern Mississippi.Crossref | GoogleScholarGoogle Scholar |
Persson, L, and De Roos, A. M. (2006). Food-dependent individual growth and population dynamics in fishes. Journal of Fish Biology 69, 1–20.
Phillips, B., and Shine, R. (2004). Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proceedings of the National Academy of Sciences of the United States of America 101, 17150–17155.
| 1:CAS:528:DC%2BD2cXhtFagu7bK&md5=5f8b030da8b39a971c8537900cc081fdCAS | 15569943PubMed |
Phillips, B. L., and Shine, R. (2006). An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proceedings of the Royal Society of London – Series B: Biological Sciences 273, 1545–1550.
Porter, S. D., and Savignano, D. A. (1990). Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71, 2095–2106.
| Invasion of polygyne fire ants decimates native ants and disrupts arthropod community.Crossref | GoogleScholarGoogle Scholar |
Reznick, D. N., and Endler, J. A. (1982). The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160–177.
| The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata).Crossref | GoogleScholarGoogle Scholar |
Ricklefs, R. E. (1984). The optimization of growth rate in altricial birds. Ecology 65, 1602–1616.
| The optimization of growth rate in altricial birds.Crossref | GoogleScholarGoogle Scholar |
Romero, L. M., and Wikelski, M. (2001). Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proceedings of the National Academy of Sciences, USA 98, 7366–7370.
| Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWmurs%3D&md5=33c29276be7a91b00e9f0d07abf9de91CAS |
Sanchez-Pena, S. R., Patrock, R. J. W., and Gilbert, L. A. (2005). The red imported fire ant is now in Mexico: documentation of its wide distribution along the Texas–Mexico border. Entomological News 116, 363–366.
Schmidt, J. O. (1990). Hymenopteran venoms: striving toward the ultimate defense against vertebrates. In ‘Insect defenses: adaptive mechanisms and strategies of prey and predators.’ (Eds D. L. Evans and J. O. Schmidt.) pp. 387–419. (State University of New York Press: Albany, NY.)
Schmidt, P. J., Sherbrooke, W. C., and Schmidt, J. O. (1989). The detoxification of ant (Pogonomyrmex) venom by a blood factor in horned lizards (Phrynosoma). Copeia 1989, 603–607.
| The detoxification of ant (Pogonomyrmex) venom by a blood factor in horned lizards (Phrynosoma).Crossref | GoogleScholarGoogle Scholar |
Semlitsch, R. D. (1990). Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Canadian Journal of Zoology 68, 1027–1030.
| Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation.Crossref | GoogleScholarGoogle Scholar |
Shine, R., and Schwarzkopf, L. (1992). The evolution of reproductive effort in lizards and snakes. Evolution 46, 62–75.
| The evolution of reproductive effort in lizards and snakes.Crossref | GoogleScholarGoogle Scholar |
Sih, A. (1985). Evolution, predator avoidance, and unsuccessful predation. American Naturalist 125, 153–157.
| Evolution, predator avoidance, and unsuccessful predation.Crossref | GoogleScholarGoogle Scholar |
Sih, A., Ziemba, R., and Harding, K. C. (2000). New insights on how temporal variation in predation risk shapes prey behavior. Trends in Ecology & Evolution 15, 3–4.
| New insights on how temporal variation in predation risk shapes prey behavior.Crossref | GoogleScholarGoogle Scholar |
Stoks, R. (1999). Autotomy shapes the trade-off between seeking cover and foraging in larval damselflies. Behavioral Ecology and Sociobiology 47, 70–75.
| Autotomy shapes the trade-off between seeking cover and foraging in larval damselflies.Crossref | GoogleScholarGoogle Scholar |
Suarez, A. V., and Case, T. J. (2002). Bottom-up effects on persistence of a specialist predator: ant invasions and horned lizards. Ecological Applications 12, 291–298.
| Bottom-up effects on persistence of a specialist predator: ant invasions and horned lizards.Crossref | GoogleScholarGoogle Scholar |
Talent, L. G., Dumont, J. N., Bantle, J. A., Janz, D. M., and Talent, S. G. (2002). Evaluation of western fence lizards (Sceloporus occidentalis) and eastern fence lizards (Sceloporus undulatus) as laboratory reptile models for toxicology investigations. Environmental Toxicology and Chemistry 21, 899–905.
| 1:CAS:528:DC%2BD38XktlWltL8%3D&md5=b1ef309a0025e8fda4f9d5f3e266fda9CAS | 12013135PubMed |
Tinkle, D. W., and Dunham, A. E. (1986). Comparative life histories of two syntopic sceloporine lizards. Copeia 1986, 1–18.
| Comparative life histories of two syntopic sceloporine lizards.Crossref | GoogleScholarGoogle Scholar |
Tschinkel, W. R. (2006). ‘The fire ants.’ (Harvard University/Belknap Press: Cambridge, MA.)
Vermeij, G. J. (1982). Unsuccessful predation and evolution. American Naturalist 120, 701–720.
| Unsuccessful predation and evolution.Crossref | GoogleScholarGoogle Scholar |
Walls, S. C., and Jaeger, R. G. (1987). Aggression and exploitation as mechanisms of competition in larval salamanders. Canadian Journal of Zoology 65, 2938–2944.
| Aggression and exploitation as mechanisms of competition in larval salamanders.Crossref | GoogleScholarGoogle Scholar |
Warner, D. A., and Andrews, R. M. (2002). Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biological Journal of the Linnean Society. Linnean Society of London 76, 105–124.
| Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards.Crossref | GoogleScholarGoogle Scholar |
