Abstract
Parasites may impair host behavior in ways that reduce host fitness, especially when access to territories or mates becomes disrupted. Western fence lizards (Sceloporus occidentalis) are a key host to western blacklegged ticks (Ixodes pacificus). Males are highly aggressive during the mating season, competing with rivals through displays of color badges, pushups, and other behaviors. We hypothesized that experimental tick infestation diminishes the performance of male western fence lizards in intrasexual contests, via either blood loss, damage to sensory structures, or both. We infested adult males with larval ticks for 7 to 10 days, staged contests between infested and quality-matched control males, and measured their behavior in enclosure arenas. Infested lizards were less aggressive and exhibited decreased hematocrit, compared to non-infested animals. We found no relationships between aggression and either body size or blue ventral badge color traits, for either infested or uninfested males. There was also no effect of tick attachment location and hemoparasite infection on host contest behavior. This is the first demonstration of the impact of I. pacificus parasitism on intraspecific interactions of western fence lizards and suggests that tick infestation has substantial impacts on lizard fitness. Because I. pacificus rely heavily on these lizards for blood meals and dispersal, these impacts could also influence the abundance of ticks and the pathogens they vector.
Significance statement
Parasitism frequently impairs host behavior. We investigated the effect of blacklegged tick parasitism on western fence lizard contest behavior using a lab-based manipulation experiment. We demonstrated that tick infestation reduced lizard aggressiveness, which may lead to territory loss and reduced mating opportunities in the wild. We found no evidence that host body size or coloration are correlated with aggression. This study adds to a growing body of evidence that tick parasitism is costly for lizards, while demonstrating the usefulness of manipulation experiments to understand host-parasite interactions.
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Data availability
The datasets generated and/or analyzed during the current study are available in the Dryad repository, https://datadryad.org/stash/share/kARmkdRbTxF4u3BqN1PCbpiiRneFQ0CvL_IUeYG2AC4.
References
Arnold EN (1986) Mite pockets of lizards, a possible means of reducing damage by ectoparasites. Biol J Linn Soc 29:1–21
Arnott G, Elwood RW (2009) Assessment of fighting ability in animal contests. Anim Behav 77:991–1004
Ayala SC (1970) Lizard malaria in California; description of a strain of Plasmodium mexicanum, and biogeography of lizard malaria in western North America. J Parasitol 56:417–425
Balenger SL, Zuk M (2014) Testing the Hamilton-Zuk hypothesis: past, present, and future. Integr Comp Biol 54:601–613
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399
Binning SA, Roch DG, Layton C (2013) Ectoparasites increase swimming costs in a coral reef fish. Biol Lett 9:20120927
Binning SA, Shaw AK, Roche G (2018) Parasites and host performance: incorporating infection into our understanding of animal movement. Integr Comp Biol 57:267–280
Bonorris JS, Ball GH (1955) Schellackia occidentalis n.sp., a blood-inhabiting coccidian found in lizards in Southern California. J Protozool 2:31–34
Borgia G, Collis K (1990) Parasites and bright male plumage in the satin bowerbird (Ptilonorhynchus violaceus). Am Zool 30:279–285
Borucinska JD, Benz GW, Whiteley HE (1998) Ocular lesions associated with attachment of the parasitic copepod Ommatokoita elongate (Grant) to corneas of Greenland sharks, Somniosus microcephalus (Block & Schneider). J Fish Dis 21:415–422
Brain C, Bohrmann R (1992) Tick infestation of baboons (Papio ursinus) in the Namib Desert. J Wildl Dis 28:188–191
Brandt Y (2003) Lizard threat display handicaps endurance. Proc R Soc Lond B 270:1061–1068
Brown RN, Lane RS (1992) Lyme disease in California: a novel enzootic transmission cycle of Borrelia burgdorferi. Science 256:1439–1442
Burgdorfer W, Barbour AG, Hayes S, Benach JL, Grunwaldt E, Davis JP (1982) Lyme disease – a tick-borne spirochetosis? Science 216:1317–1319
Carpenter CC (1978) Comparative display behavior in the genus Sceloporus (Iguanidae). Contrib Biol Geol 18:1–72
Clayton DH (1991) The influence of parasites on host sexual selection. Parasitol Today 7:329–334
Clover JR, Lane RS (1995) Evidence implicating nymphal Ixodes pacificus (Acari: Ixodidae) in the epidemiology of Lyme disease in California. Am J Trop Med Hyg 53:237–240
Cooper WE, Burns N (1987) Social significance of ventrolateral coloration in the fence lizard, Sceloporus undulatus. Anim Behav 35:526–532
Costello AB, Osborne JW (2005) Best practices in exploratory factor analysis: four recommendations for getting the most from your analysis. Pract Assess Res Eval 10:1–9
Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46–57
de Lanuza G, Carazo P, Font E (2014) Colours of quality: structural (but not pigment) coloration informs about male quality in a polychromatic lizard. Anim Behav 90:73–81
Deen CM, Hutchison VH (2001) Effects of lipopolysaccharide and acclimation temperature on induce behavioral fever in juvenile Iguana iguana. J Therm Biol 26:55–63
Doucet SM, Meadows MG (2009) Iridescence: a functional perspective. J Roy Soc Interf 6:S115–S132
Ducrest A, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510
Dunlap KT, Mathies T (1993) Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards. Copeia 1993:1045–1048
Eisen RJ, Eisen L, Lane RS (2001) Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentalis) in Northern California: temporal trends and environmental correlates. J Parasitol 87:1301–1307
Eisen L, Eisen RJ, Lane RS (2004) The roles of birds, lizards, and rodents as hosts for the western black-legged tick Ixodes pacificus. J Vector Ecol 29:295–308
Engbretson GA, Livezey RL (1972) The effects of aggressive display on body temperature in the fence lizard Sceloporus occidentalis occidentalis Baird and Girard. Physiol Zool 45:247–254
Eshoo MW, Carolan HE, Massire C, Chou DM, Crowder CD, Rounds MA, Philipson CA, Schutzer SE, Ecker DJ (2015) Survey of Ixodes pacificus ticks in California reveals diversity of microorganisms and a novel widespread Anaplasmataceae species. PLoS ONE 10:e0135828
Fawcett TW, Mowles SL (2013) Assessment of fighting ability need not be cognitively complex. Anim Behav 86:e1–e7
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 136:603–622
Forbes MRL (1993) Parasitism and host reproductive effort. Oikos 67:444–450
Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330
Furman DP, Loomis EC (1984) The ticks of California (Acari: Ixodida). University of California Press, Berkeley
Garland T, Hankins E, Huey RB (1990) Locomotor capacity and social dominance in male lizards. Funct Ecol 4:243–250
Goldberg SR, Bursey CR (1991) Integumental lesions caused by ectoparasites in a wild population of the side-blotched lizard (Uta stansburiana). J Wildl Dis 27:68–73
Goldberg SR, Bursey CR, Cheam H (1998) Composition of helminth communities in montane and lowland populations of the western fence lizard, Sceloporus occidentalis from Los Angeles County, California. Am Midl Nat 140:186–191
Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B 205:581–598
Haenel GJ, Smith LC, John-Alder HB (2003) Home-range analysis in Sceloporus undulatus (eastern fence lizard). I. Spacing patterns and the context of territorial behavior. Copeia 2003:99–112
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
Hamilton PS, Gaalema DE, Laage SL, Sullivan BK (2005) A photographic method for quantifying color characteristics and color patch dimensions in lizards. Herpetol Rev 36:402–406
Hart BJ (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav R 12:123–137
Herbison REH (2017) Lessons in mind control: trends in research on the molecular mechanisms behind parasite-host behavioral manipulation. Front Ecol Evol 5:102
Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2006) A Lego system for conditional inference. Am Stat 60:257–263
Huyghe K, Vanhooydonck B, Scheers H, Molina-Borja M, Van Damme R (2005) Morphology, performance and fighting capacity in male lizards, Gallotia galloti. Funct Ecol 19:800–807
Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev 70:1–65
Kaiser HF, Rice J (1974) Little Jiffy, Mark IV. Educ Psychol Meas 34:111–117
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
Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79:441–449
Kortet R, Hedrik AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458
Kuo MM, Lane RS, Giclas PC (2000) A comparative study of mammalian and reptilian alternative pathway of complement-mediated killing of the Lyme disease spirochete (Borrelia burgdorferi). J Parasitol 86:1223–1228
Lafferty KD, Shaw JC (2013) Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 216:56–66
Lane RS, Loye JE (1989) Lyme disease in California: interrelationship of Ixodes pacificus (Acari: Ixodidae), the western fence lizard (Sceloporus occidentalis), and Borrelia burgdorferi. J Med Entomol 26:272–278
Lane RS, Quistad GB (1998) Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). J Parasitol 84:29–34
Lane RS, Mun J, Stubbs HA (2010) Horizontal and vertical movements of host-seeking Ixodes pacificus (Acari: Ixodidae) nymphs in a hardwood forest. J Vector Ecol 34:252–266
Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:8–13
Lumbad AS, Vredevoe LK, Taylor EN (2011) Season and sex of host affect intensities of ectoparasites in western fence lizards (Sceloporus occidentalis) on the Central Coast of California. Southwest Nat 56:369–377
Maksimowich DS, Mathis A (2000) Parasitized salamanders are inferior competitors for territories and food resources. Ethology 106:319–329
Martin TL, Huey RB (2008) Why “suboptimal” is optimal: Jensen’s inequality and ectotherm thermal preferences. Am Nat 171:e102–e118
Martin M, Meylan S, Haussy C, Decencière B, Perret S, Le Galliard J (2016) UV color determines the issue of conflicts but does not covary with individual quality in a lizard. Behav Ecol 27:262–270
McElroy EJ, de Buron I (2014) Host performance as a target of manipulation by parasites: a meta-analysis. J Parasitol 100:399–410
Megía-Palma R, Martínez J, Merino S (2014) Molecular characterization of haemococcidia genus Schellackia (Apicomplexa) reveals the polyphyletic origin of the family Lankesterellidae. Zool Scr 43:304–312
Megía-Palma R, Martínez J, Merino S (2016a) A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. Sci Nat 103:52
Megía-Palma R, Martínez J, Merino S (2016b) Structural- and carotenoid-based throat colour patches in males of Lacerta schreiberi reflect different parasitic diseases. Behav Ecol Sociobiol 70:2017–2025
Megía-Palma R, Martínez J, Paranjpe D, Damico V, Rocío A, Palacios MG, Cooper R, Ferri-Yanez F, Sinervo B, Merino S (2017) Phylogenetic analyses reveal that Schellackia parasites (Apicomplexa) detected in American lizards are closely related to the genus Lankesterella: is the range of Schellackia restricted to the Old World? Parasite Vector 10:470
Megía-Palma R, Paranjpe D, Reguera S, Martínez J, Cooper RD, Blaimont P, Merino S, Sinervo B (2018) Multiple color patches and parasites in Sceloporus occidentalis: differential relationships by sex and infection. Curr Zool 64:703–711
Megía-Palma R, Paranjpe D, Blaimont P, Cooper R, Sinervo B (2020) To cool or not to cool? Intestinal coccidians disrupt the behavioral hypothermia of lizards in response to tick infestation. Ticks Tick-Borne Dis 11:101275
Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20
Morrison RL, Frost-Mason SK (1991) Ultrastructural analysis of iridophore organellogenesis in a lizard, Sceloporus graciosus (Reptilia: Phrynosomatidae). J Morphol 209:229–239
Morrison RL, Rand MS, Frost-Mason SK (1995) Cellular basis of color differences in three morphs of the lizard Sceloporus undulatus erythrocheilus. Copeia 1995:397–408
Musante AR, Pekins PJ, Scarpitti DL (2007) Metabolic impacts of winter tick infestations on calf moose. Alces 43:101–110
Olsson M (1994) Nuptial coloration in the sand lizard, Lacerta agilis: an intra-sexually selected cue to fighting ability. Anim Behav 48:607–613
Olsson M, Wapstra E, Madsen T, Silverin B (2000) Testosterone, ticks, and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proc R Soc Lond B 267:2339–2343
Ossip-Drahos AG, Oyola Morales JR, Vital-García C, Zúñiga-Vega JJ, Hews DK, Martins EP (2016) Shaping communicative colour signals over evolutionary time. R Soc Open Sci 3:160728
Ossip-Drahos AG, Berry NJ, King CM, Martins EP (2018) Information-gathering as a response to manipulated signals in the eastern fence lizard, Sceloporus undulatus. Ethology 124:684–690
Pittman W, Pollock NB, Taylor EN (2013) Effect of host lizard anemia on host choice and feeding rate of larval western black-legged ticks (Ixodes pacificus). Exp Appl Acarol 61:471–479
Pollock NB, Vredevoe LK, Taylor EN (2012) How do host sex and reproductive state affect host preference and feeding duration of ticks? Parasitol Res 111:897–907
Quinn VS, Hews DK (2003) Positive relationship between abdominal coloration and dermal melanin density in phrynosomatid lizards. Copeia 2003:858–864
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/. Accessed 1 June 2018
Rau ME (1984) Loss of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology 88:371–373
Regal PJ (1971) Long term studies with operant conditioning techniques of temperature regulation patterns in reptiles. J Physiol-Paris 63:403–406
Ressel S, Schall JJ (1989) Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78:158–164
Revelle W (2018) Psych: procedures for personality and psychological research, https://CRAN.R-project.org/package=psych. Accessed 1 June 2018
Robbins TR, Pruitt JN, Straub LE, McCoy ED, Mushinsky HR (2010) Transgressive aggression in Sceloporus hybrids confers fitness through advantages in male agonistic encounters. J Anim Ecol 79:137–147
Rosenqvist G, Johansson K (1995) Male avoidance of parasitized females explained by direct benefits in a pipefish. Anim Behav 49:1039–1045
Salkeld DJ, Lane RS (2010) Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology 91:293–298
Salvador A, Veiga JP, Martin J, Lopez P, Abelenda M, Puerta M (1996) The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasite infestation. Behav Ecol 7:145–150
Salvador A, Veiga JP, Civantos E (1999) Do skin pockets of lizards reduce the deleterious effects of ectoparasites? An experimental study with Psammodromus algirus. Herpetologica 55:1–7
San José LL, Roulin A (2018) Toward understanding the repeated occurrence of associations between melanin-based coloration and multiple phenotypes. Am Nat 192:111–130
Schall JJ (1982) Lizard malaria: parasite-host ecology. In: Huey RB, Pianka ER, Schoener TW (eds) Lizard ecology: studies on a model organism. Harvard University Press, Cambridge, pp 84–100
Schall JJ (1983) Lizard malaria: cost to vertebrate host’s reproductive success. Parasitology 87:1–6
Schall JJ, Dearing MD (1987) Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidentalis. Oecologia 73:389–392
Schall JJ, Houle PR (1992) Malarial parasitism and home range and social status of male western fence lizards, Sceloporus occidentalis. J Herpetol 26:74–76
Schall JJ, Sarni GA (1987) Malarial parasitism and the behavior of the lizard, Sceloporus occidentalis. Copeia 1987:84–93
Schall JJ, Bennett AF, Putnam RW (1982) Lizards infected with malaria: physiological and behavioral consequences. Science 217:1057–1059
Schindelin J, Aganda-Carreras I, Frise E et al (2012) Fiji – an open source platform for biological image analysis. Nat Methods 9:676–682
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Schoeler GB, Wikel S (2001) Modulation of host immunity by haematophagous arthropods. Ann Trop Med Parasitol 95:755–771
Scholnick DA, Manivanh RV, Savenkova OD, Bates TG, McAlexander SL (2010) Impact of malarial infection on metabolism and thermoregulation in the fence lizard Sceloporus occidentalis from Oregon. J Herpetol 44:634–640
Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction-immunity trade-offs in insects. Annu Rev Entomol 61:239–256
Seddon RJ, Hews DK (2016) Phenotypic correlates of melanization in two Sceloporus occidentalis (Phrynosomatidae) populations: behavior, androgens, stress reactivity, and ectoparasites. Physiol Behav 163:70–80
Seddon RJ, Hews DK (2018) Correlates of melanization in multiple high- and low-elevation populations of the lizard, Sceloporus occidentalis: behavior, hormones, and parasites. J Exp Zool 327:481–492
Sheldahl LA, Martins EP (2000) The territorial behavior of the western fence lizard, Sceloporus occidentalis. Herpetologica 56:469–479
Stamps JA, Krishnan VV (1994) Territory acquisition in lizards: I. First encounters. Anim Behav 47:1375–1385
Stamps JA, Krishnan VV (1998) Territory acquisition in lizards: IV. Obtaining high status and exclusive home ranges. Anim Behav 55:461–472
Stebbins RC (2003) A field guide to western reptiles and amphibians, 3rd edn. Houghton Mifflin, New York
Stephenson JF, Stevens M, Troscianko J, Jokela J (2020) The size, symmetry, and color saturation of a male guppy’s ornaments forecast his resistance to parasites. Am Nat 196:597–608 (published online). https://doi.org/10.1086/711033)
Swei A, Ostfeld RS, Lane RS, Briggs CJ (2011) Impact of the experimental removal of lizards on Lyme disease risk. Proc R Soc Lond B 278:2970–2978
Swierk L, Langkilde T (2013) Bearded ladies: females suffer fitness consequences when bearing male traits. Biol Lett 9:2030644
Swierk L, Ridgway M, Langkilde T (2012) Female lizards discriminate between potential reproductive partners using multiple male traits when territory cues are absent. Behav Ecol Sociobiol 66:1033–1043
Torio AJ (1992) Effect of parasitic infection on male color pattern and female choice in guppies. Behav Ecol 3:346–351
Vardo AM, Wargo AR, Schall JJ (2005) PCR detection of lizard malaria parasites: prevalence of Plasmodium infections with low-level parasitemia differs by site and season. J Parasitol 91:1509–1511
Wieczorek M, Rektor R, Najbar B, Morelli F (2020) Tick parasitism is associated with home range area in the sand lizard, Lacerta agilis. Amphibia-Reptilia (published online). https://doi.org/10.1163/15685381-bja10018)
Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Am Zool 38:191–206
Wojan EM, Carreiro NC, Clendenen DA, Neldner HM, Castillo C, Bertram SM, Kolluru GR (2019) The effects of commonly used anaesthetics on colour measurements across body regions in the poeciliid fish, Girardinus metallicus. J Fish Biol 95:1320–1330
Yasir I, Qin JG (2009) Effect of light intensity on color performance of false clownfish, Amphiprion ocellaris Cuvier. J World Aquacult Soc 40:337–350
Zahavi A (1975) Mate selection – a selection for a handicap. J Theor Biol 53:205–214
Acknowledgments
We thank the two anonymous reviewers whose feedback greatly improved the manuscript, Emily Taylor for her help in conceptualizing this project, David Clendenen for photography, Heather Neldner for assistance with animal husbandry, Doug Brewster for help in constructing animal housing, Aaron Lazanoff for providing cattle for tick feedings, Christy Strand for providing video surveillance cameras, and John Walker for feedback on statistical methods. We also thank Rebeca Almeida, Eric Gonzales, Kei Iemori, Fiona Kelly, Julius Larion, Connor Maldonado, Andrew Morris, Lucy Ramirez, Esmeralda Sanchez, Jenna Van Mouwerik, and other members of the Vredevoe lab for their general assistance.
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Custom code created during the current study is available in the Dryad repository, https://datadryad.org/stash/share/kARmkdRbTxF4u3BqN1PCbpiiRneFQ0CvL_IUeYG2AC4.
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Funding came from the Baker/Koob Endowment and the California Polytechnic State University College Based Fees.
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All applicable international, national, and/or institutional guidelines for the use of animals were followed. Use of animals was approved by the California Polytechnic State University, San Luis Obispo, Institutional Animal Care and Use Committee (protocol #1609), and a California Department of Fish and Wildlife permit (#SC-013426 to DL). Consent to participate is not applicable.
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Lanser, D.M., Vredevoe, L.K. & Kolluru, G.R. Tick parasitism impairs contest behavior in the western fence lizard (Sceloporus occidentalis). Behav Ecol Sociobiol 75, 40 (2021). https://doi.org/10.1007/s00265-021-02980-y
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DOI: https://doi.org/10.1007/s00265-021-02980-y