Abstract
Simultaneously defending against predators, stymieing competitors, and generating immune responses can impose conflicting demands for host species caught in the entanglement of a food web. Host immunity is not only shaped by direct interactions among species, but also many indirect cascading effects. By reducing competition, predators in particular can affect resource acquisition necessary for hosts to mount energetically costly immune responses. However, identifying the links between predators and host immune responses determined by resource acquisition is a complex affair, because predators can (1) reduce host density and thus competition among hosts, (2) exert non-consumptive trait-mediated effects on host resource acquisition behavior, and (3) generate natural selection on host resource acquisition behavior. To examine the relative contributions of these potential predator driven density- and trait-mediated effects on a key aspect of immune function (total phenoloxidase activity, total PO), we conducted mesocosm and field experiments with larval damselflies (Enallagma signatum) and their dominant fish predator (Lepomis macrochirus). Although we expected to observe declines in total PO activity with increases in damselfly density, we found no relationship between density and total PO activity. We also found no support for the prediction that total PO activity would vary as a result of either non-consumptive trait-mediated effects or selection on damselfly foraging activity underlying resource acquisition. Despite the lack of trait- or density-mediated effects, we did find that total PO activity increased with damselfly prey density among lakes, implying resource limitation for this aspect of immune function. These unexpected results point to the need to better understand the ecological conditions whereby predators and competitors constrain immune functions necessary for species to defend themselves in complex food webs.
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Availability of data and materials
The datasets analyzed during the current study are available in the DataDryad repository, https://doi.org/10.5061/dryad.0p2ngf21t.
Code availability
The code used in the current study is available in the DataDryad repository, https://doi.org/10.5061/dryad.0p2ngf21t.
References
Adamo SA (2017) Stress responses sculpt the insect immune system, optimizing defense in an ever-changing world. Dev Comp Immunol 66:24–32
Anholt B (1990) An experimental separation of interference and exploitative competition in larval damselfly. Ecology 71:1483–1493
Anholt BR (1994) Cannibalism and early instar survival in a larval damselfly. Oecologia 99:60–65
Barnes AI, Siva-Jothy MT (2000) Density dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc R Soc B 267:177–182
Benkman CW (2013) Biotic interaction strength and the intensity of selection. Ecol Lett 16:1054–1060
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brodin T, Johansson F (2004) Conflicting selection pressures on the growth/predation-risk trade-off in a damselfly. Ecology 85:2927–2932
Bruijning M, ten Berge ACM, Jongejans E (2018) Population-level responses to temperature, density and clonal differences in Daphnia magna as revealed by integral projection modelling. Funct Ecol 32:2407–2422
Budischak SA, Cressler CE (2018) Fueling defense: effects of resources on the ecology and evolution of tolerance to parasite infection. Front Immunol 9:2453
Budischak SA, Hansen CB, Caudron Q, Garnier R, Kartzine T, Pelczer I, Cressler CE, van Leeuwen A, Graham AL (2018) Feeding immunity: physiological and behavioral responses to infection and resource limitation. Front Immunol 8:1914
Campero M, De Block M, Ollevier F, Stoks R (2008) Correcting the short-term effect of food deprivation in a damselfly: mechanisms and costs. J Anim Ecol 77:66–73
Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315
Chesson P, Kuang J (2008) The interaction between predation and competition. Nature 456:235–238
Contreras-Garduño J, Canales-Lazcano J, Córdoba-Aguilar A (2006) Wing pigmentation, immune ability, fat reserves and territorial status in males of the rubyspot damselfly, Hetaerina americana. J Ethol 24:165–173
Córdoba-Aguilar A, Ruiz-Silva D, Munguía-Steyer R, Lanz-Mendoza H (2011) Do reproductive activities compromise immunological competence as measured by phenoloxidase activity? Field and experimental manipulation in females of two damselfly species. Ecol Entomol 36:335–342
De Block M, Stoks R (2004) Life-history variation in relation to time constraints in a damselfly. Oecologia 140:68–75
De Block M, Stoks R (2008) Short-term larval food stress and associated compensatory growth reduce adult immune function in a damselfly. Ecol Entomol 33:796–801
Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745
Duong TM, McCauley SJ (2016) Predation risk increases immune response in a larval dragonfly (Leucorrhinia intacta). Ecology 97:1605–1610
Elliot SL, Hart AG (2010) Density-dependent prophylactic immunity reconsidered in the light of host group living and social behavior. Ecology 91:65–72
Fedorka KM, Copeland EK, Winterhalter WE (2013) Seasonality influences cuticle melanization and immune defense in a cricket: support for a temperature-dependent immune investment hypothesis in insects. J Exp Biol 216:4005–4010
Forbes KM, Mappes T, Sironen T, Strandin T, Stuart P, Meri S, Vapalahti O, Henttonen H, Huitu O (2016) Food limitation constrains host immune responses to nematode infections. Biol Lett 12:1220160471
Gershman SN (2008) Sex-specific differences in immunological costs of multiple mating in Gryllus vocalis field crickets. Behav Ecol 19:810–815
González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16
Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155:435–453
Hite JL, Cressler CE (2019) Parasite-mediated anorexia and nutrition modulate virulence evolution. Integr Comput Biol 59:1264–1274
Iserbyt A, Van Gossum H, Stoks R (2012) Biogeographical survey identifies consistent alternative physiological optima and a minor role for environmental drivers in maintaining a polymorphism. PLoS ONE 7:e32648
Jiménez-Cortés JG, Serrano-Meneses MA, Córdoba-Aguilara A (2012) The effects of food shortage during larval development on adult body size, body mass, physiology and developmental time in a tropical damselfly. J Insect Physiol 58:318–326
Johansson F, Rowe L (1999) Life history and behavioral responses to time constraints in a damselfly. Ecology 80:1242–1252
Kobler A, Klefoth T, Mehner T, Arlinghaus R (2009) Coexistence of behavioural types in an aquatic top predator: A response to resource limitation? Oecologia 161:837–847
Kong H, Dong C, Tian Z, Mao N, Wang C, Cheng Y, Zhang L, Jiang X, Luo L (2018) Altered immunity in crowded Mythimna separata is mediated by octopamine and dopamine. Sci Rep 8:1–10
Kortet R, Rantala M, Hedrick A (2007) Boldness in anti-predator behaviour and immune defence in field crickets. Evol Ecol Res 9:185–197
Kristan DM (2008) Calorie restriction and susceptibility to intact pathogens. Age 30:147–156
Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: Just what is the cost of immunity? Oikos 88:87–98
Marmaras VJ, Charalambidis ND, Zervas CG (1996) Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Arch Insect Biochem Physiol 31:119–133
McPeek MA (1990) Behavioral differences between Enallagma species (Odonata) influencing differential vulnerability to predators. Ecology 71:1714–1726
McPeek MA (1998) The consequences of changing the top predator in a food web: a comparative experimental approach. Ecol Monogr 68:1–23
McPeek MA (2004) The growth/predation risk trade-off: So what is the mechanism? Am Nat 163:E88–E111
McPeek MA (2017) The ecological dynamics of natural selection: traits and the coevolution of community structure. Am Nat 189:E91–E117
McPeek MA, Crowley PH (1987) The effects of density and relative size on the aggressive behaviour, movement and feeding of damselfly larvae (Odonata: Coenagrionidae). Anim Behav 35:1051–1061
McPeek MA, Grace M, Richardson JML (2001) Physiological and behavioral responses to predators shape the growth predation risk trade-off in damselflies. Ecology 82:1535–1545
Mikolajewski DJ, Stoks R, Rolff J, Joop G (2008) Predators and cannibals modulate sex-specific plasticity in life-history and immune traits. Funct Ecol 22:114–120
Miller GA, Simpson SJ (2010) Isolation from a marching band increases haemocyte density in wild locusts (Chortoicetes terminifera). Ecol Entomol 35:236–239
Mlynarek JJ, Iserbyt A, Nagel L, Forbes MR (2015) Differential water mite parasitism, phenoloxidase activity, and resistance to mites are unrelated across pairs of related damselfly species. PLoS ONE 10:e0115539
Murray RL, Tah S, Koprivnikar J, Rowe L, McCauley SJ (2020) Exposure to potentially cannibalistic conspecifics induces an increased immune response. Ecol Entomol 45:355–363
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-models. Methods Ecol Evol 4:133–142
Ousterhout BH, Graham SR, Hasik AZ, Serrano M, Siepielski AM (2018) Past selection impacts the strength of an aquatic trophic cascade. Funct Ecol 32:1554–1562
Ousterhout BH, Serrano M, Bried JT, Siepielski AM (2019) A framework for linking competitor ecological differences to coexistence. J Anim Ecol 88:1534–1548
Piesk M, Karl I, Franke K, Fischer K (2013) High larval density does not induce a prophylactic immune response in a butterfly. Ecol Entomol 38:346–354
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reznick D, Nunneya L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425
Rigby MC, Jokela J (2000) Predator avoidance and immune defence: costs and tradeoffs in snails. Proc R Soc B 267:171–176
Sadd BM, Schmid-Hempel P (2009) PERSPECTIVE: principles of ecological immunology. Evolut Appl 2:113–121
Sadd BM, Siva-Jothy MT (2006) Self-harm caused by an insect’s innate immunity. Proc R Soc B 273:2571–2574
Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
Siepielski AM, McPeek MA (2013) Niche versus neutrality in structuring the beta diversity of damselfly assemblages. Freshw Biol 58:758–768
Siepielski AM, Hung K-L, Bein EEB, McPeek MA (2010) Experimental evidence for neutral community dynamics governing an insect assemblage. Ecology 91:847–857
Siepielski AM, Mertens AN, Wilkinson BL, McPeek MA (2011) Signature of ecological partitioning in the maintenance of damselfly diversity. J Anim Ecol 80:1163–1173
Siepielski AM, Wang J, Prince G (2014) Nonconsumptive predator-driven mortality causes natural selection on prey. Evolution 68:696–704
Siepielski AM, Fallon E, Boersma K (2016) Predator olfactory cues generate a foraging–predation trade-off through prey apprehension. R Soc Open Sci 3:150537
Siepielski AM, Hasik AZ, Ping T, Serrano M, Strayhorn K, Tye SP (2020) Predators weaken prey intraspecific competition through phenotypic selection. Ecol Lett 23:951–961
Siva-Jothy MT, Thompson JJW (2002) Short-term nutrient deprivation affects immune function. Physiol Entomol 27:206–212
Siva-Jothy MT, Moret Y, Rolff J (2005) Insect immunity: an evolutionary ecology perspective. Adv Insect Physiol 32:1–48
Smith IM, Cook DR, Smith BP (2010) Water mites (Hydrachnidiae) and other arachnids. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, pp 485–586
Srygley RB, Jaronski ST (2011) Immune response of Mormon crickets that survived infection by Beauveria bassiana. J Insect Physiol 58:342–347
Stahlschmidt ZR, Jeong N, Johnson D, Meckfessel N (2020) From phenoloxidase to fecundity: food availability does not influence the costs of oxidative challenge in a wing-dimorphic cricket. J Comp Physiol B 190:17–26
Start D (2018) Ontogeny and consistent individual differences mediate trophic interactions. Am Nat 192:301–310
Start D, Gilbert B (2017) Predator personality structures prey communities and trophic cascades. Ecol Lett 20:366–374
Stearns SC (1992) The evolution of life histories. Chapman and Hall, New York
Stoks R (2001) Food stress and predator-induced stress shape developmental performance in a damselfly. Oecologia 127:222–229
Stoks R, McPeek MA (2003) Antipredator behavior and physiology determine Lestes species turnover along the pond-permanence gradient. Ecology 84:3327–3338
Stoks R, McPeek MA (2006) A tale of two diversifications: reciprocal habitat shifts to fill ecological space along the pond permanence gradient. Am Nat 168:S50–S72
Stoks R, McPeek MA, Mitchell JL (2003) Evolution of prey behavior in response to changes in predation regime: damselflies in fish and dragonfly lakes. Evolution 57:574–585
Stoks R, De Block M, Slos S, Van Doorslaer W, Rolff J (2006) Time constraints mediate predator-induced plasticity in immune function, condition, and life history. Ecology 84:809–815
Strobbe F, Stoks R (2004) Life history reaction norms to time constraints in a damselfly: differential effects on size and mass. Biol J Lin Soc 83:187–196
Strobbe F, McPeek MA, De Block M, De Meester L, Stoks R (2009) Survival selection on escape performace and it underlying phenotypic traits: a case of many-to-one mapping. J Evol Biol 22:1172–1182
Strobbe F, McPeek MA, De Block M, Stoks R (2011) Fish predation selects for reduced foraging activity. Behav Ecol Sociobiol 65:241–247
Svensson E, Sinervo B, Comendant T (2001) Density-dependent competition and selection on immune function in genetic lizard morphs. Proc Natl Acad Sci 98:12561–12565
Swaegers J, Strobbe F, McPeek MA, Stoks R (2017) Selection on escape performance during ecological speciation driven by predation. J Anim Behav 124:153–159
Thomas R, Hoverman JT, Halsead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 91:1900–1907
Tollrian R, Duggen S, Weiss LC, Laforsch C, Kopp M (2015) Density-dependent adjustment of inducible defenses. Sci Rep 5:1–9
Tye SP, Blaske BK, Siepielski AM (2020) Population-level variation of digestive physiology costs of mounting an immune response in damselflies. Ecol Entomol 45:635–643
van der Most PJ, de Jong B, Parmentier HK, Verhulst S (2010) Trade-off between growth and immune function: a meta-analysis of selection experiments. Funct Ecol 2:74–80
Van Dievel M, Janssens L, Stoks R (2016) Short- and long-term behavioural, physiological and stoichiometric responses to predation risk indicate chronic stress and compensatory mechanisms. Oecologia 181:347–357
Vinterstare J, Hegemann A, Nilsson PA, Hulthén K, Brönmark C (2019) Defence versus defence: Are crucian carp trading off immune function against predator-induced morphology? J Anim Ecol 88:1510–1521
Werner EE, Peacor SD (1993) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100
Wilson K, Reeson AF (1998) Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol Entomol 23:100–101
Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL (2002) Coping with crowds: density-dependent disease resistance in desert locusts. Proc Natl Acad Sci USA 99:5471–5475
Zhang J, Huang FS, Xu WY, Peng S, Duan JH, Yang S, Qiu ZW (2008) Plasmodium yoelii: correlation of up-regulated prophenoloxidase and phenoloxidases with melanization induced by the antimalarial, nitroquine. Exp Parasitol 118:308–314
Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22
Acknowledgements
We thank Kristian Forbes, Miguel Gómez-Llano, Wade Boys, and two anonymous reviewers for comments on earlier versions of this work. We also thank Mabel Serrano and Koby Strayhorn for help with experiments and Shelley Adamo, Robby Stoks, and Ria Van Houdt for help with lab work. AZH benefitted from the musical inspiration of Wind Rose. This work was supported by NSF (DEB 1748945) awarded to AMS and by Arkansas Biosciences Institute.
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This work was supported by NSF (DEB 1748945) awarded to AMS and by Arkansas Biosciences Institute.
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AMS designed the study. All authors collected data, and both AZH and AMS performed modeling work and analyzed data. AZH wrote the first draft of the manuscript, and all authors contributed substantially to revisions.
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Hasik, A.Z., Tye, S.P., Ping, T. et al. A common measure of prey immune function is not constrained by the cascading effects of predators. Evol Ecol 37, 13–30 (2023). https://doi.org/10.1007/s10682-021-10124-x
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DOI: https://doi.org/10.1007/s10682-021-10124-x