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Prey-predator interactions between two intraguild predators modulate their behavioral decisions

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Abstract

Intraguild predators can have behavioral mechanisms to maximize foraging and/or avoid predation. However, there is a lack of information about the influence of such prey-predator interactions on the daily activity of the species involved. Therefore, we investigated the daily activity of two intraguild predators, Tityus pusillus Pocock, 1893 and Ananteris mauryi Lourenço, 1982, in the presence and absence of each other. Animals were observed in three experimental conditions, containing individuals of T. pusillus (control 1), A. mauryi (control 2), and both species (treatment). In addition, we evaluated the correlation between the number of active individuals with air temperature and humidity. Our results showed that T. pusillus and A. mauryi have similar daily activity between 18:00 and 05:00 h. However, T. pusillus was more active and shifted from a sit-and-wait hunting mode to actively hunting when in the presence of A. mauryi. In contrast, under predation risk, A. mauryi did not change its level of activity but became more vigilant by reducing the frequency of rest, hydration, and mating attempts. Activity of A. mauryi was positively correlated with air humidity whereas activity of T. pusillus was negatively correlated. This work highlights the influence of intraguild predators in the behavioral decisions during daily activities of each other, indicating adaptive behaviors in both prey and predator.

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References

  • Abushama FT (1964) On the behaviour and sensory physiology of the scorpion Leiurus quinquestriatus (H. & E.). Anim Behav 12(1):140–153

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49(3):227–266

    Article  CAS  PubMed  Google Scholar 

  • Belgrad BA, Griffen BD (2016) Predator–prey interactions mediated by prey personality and predator hunting mode. Proc R Soc B 283:20160408

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Binz H, Kraft EF, Entling MH, Menzel F (2016) Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species. Chemoecology 26(4):153–162

    Article  Google Scholar 

  • Brown CA, O’Connell DJ (2000) Plant climbing behavior in the scorpion Centruroides vittatus. Am Midl Nat 144(2):406–418

    Article  Google Scholar 

  • Brownell PH, Farley RD (1979) Prey localization behaviour of the nocturnal scorpion, Paruroctonus mesaensis: orientation to substrate vibrations. Anim Behav 27:185–193

    Article  Google Scholar 

  • Carlson BE, Rowe MP (2009) Temperature and desiccation effects on the antipredator behavior of Centruroides vittatus (Scorpiones: Buthidae). J Arachnol 37(3):321–330

    Article  Google Scholar 

  • Cloudsley-Thompson JL (1962) Microclimates and the distribution of terrestrial arthropods. Annu Rev Entomol 7(1):199–222

    Article  Google Scholar 

  • 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(2):347–357

    Article  PubMed  Google Scholar 

  • Dionisio-da-Silva W, Lira AFA, Albuquerque CMR (2018) Distinct edge effects and reproductive periods of sympatric litter-dwelling scorpions (Arachnida: Scorpiones) in a Brazilian Atlantic forest. Zoology 129:17–24

    Article  PubMed  Google Scholar 

  • Fausch KD, Nakano S, Kitano S (1997) Experimentally induced foraging mode shift by sympatric charrs in a Japanese mountain stream. Behav Ecol 8(4):414–420

    Article  Google Scholar 

  • Fulton CJ, Bellwood DR (2002) Patterns of foraging in labrid fishes. Mar Ecol Prog Ser 226:135–142

    Article  Google Scholar 

  • Gavrilov I, Pusev R (2014) normtest: tests for normality. R package version 1.1. Available from: <https://CRAN.R-project.org/package=normtest>. Accessed 01 Feb 2019

  • Hadley NF (1974) Adaptational biology of desert scorpions. J Arachnol 2(1):11–23

    Google Scholar 

  • Harrell Jr. FE (2019) Hmisc: Harrell Miscellaneous. R package version 4.2-0. Available from: https://CRAN.R-project.org/package=Hmisc. Accessed: 02 April 2019

  • Hettyey A, Tóth Z, Thonhauser KE, Frommen JG, Penn DJ, Van Buskirk J (2015) The relative importance of prey-borne and predator-borne chemical cues for inducible antipredator responses in tadpoles. Oecologia 179(3):699–710

    Article  PubMed  Google Scholar 

  • Hjelle TJ (1990) Anatomy and morphology. In: Polis GA (ed) The biology of scorpions, pp. 5-30

  • Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149(4):745–764

    Article  Google Scholar 

  • Huey RB, Pianka ER (1981) Ecological consequences of foraging mode. Ecology 62(4):991–999

    Article  Google Scholar 

  • Kalinkat G, Brose U, Rall BC (2013) Habitat structure alters top-down control in litter communities. Oecologia 172(3):877–887

    Article  PubMed  Google Scholar 

  • Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299(5611):1388–1391

    Article  CAS  PubMed  Google Scholar 

  • Kondoh M (2007) Anti-predator defence and the complexity–stability relationship of food webs. P Roy Soc Lond B Bio 274(1618):1617–1624

    Google Scholar 

  • Kondoh M (2008) Building trophic modules into a persistent food web. Proc Natl Acad Sci USA 105(43):16631–16635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lira AFA, DeSouza AM, Silva Filho AAC, Albuquerque CMR (2013) Spatio-temporal microhabitat use by two co-occurring species of scorpions in Atlantic rainforest in Brazil. Zoology 116(3):182–185

    Article  PubMed  Google Scholar 

  • Lira AFA, DeSouza AM, Albuquerque CMR (2017a) Report of intraguild predation and cannibalism in scorpions (Scorpiones: Buthidae) in the Brazilian Atlantic forest. North-West J Zool e167302

  • Lira AFA, Pordeus LM, Albuquerque CMR (2017b) A new species of Ananteris (Scorpiones: Buthidae) from Caatinga biome, Brazil. Acta Arachnol 66(1):9–15

  • Lira AFA, DeSouza AM, Albuquerque CMR (2018) Environmental variation and seasonal changes as determinants of the spatial distribution of scorpion (Arachnida: Scorpiones) in Neotropical forests. Can J Zool 96(9):963–972

    Article  Google Scholar 

  • Lourenço WR (2002) Scorpions of Brazil. Les editions de l’If, Paris

    Google Scholar 

  • Lourenço WR (2012) Humiculous scorpions: on the genera Ananteris Thorell, 1891 and Microananteris Lourenço, 2004 (Scorpiones: Buthidae), with the description of a new species from French Guiana. C R Biol 335(8):555–561

    Article  PubMed  Google Scholar 

  • Lourenço WR (2015) Comments on the Ananterinae Pocock, 1900 (Scorpiones: Buthidae) and description of a new remarkable species of Ananteris from Peru. C R Biol 338(2):134–139

    Article  PubMed  Google Scholar 

  • Machan L (1968) Spectral sensitivity of scorpion eyes and the possible role of shielding pigment effect. J Exp Biol 49(1):95–105

    Article  Google Scholar 

  • Mattoni CI, García-Hernández S, Botero-Trujillo R, Ochoa JA, Ojanguren-Affilastro AA, Pinto-da-Rocha R, Prendini L (2015) Scorpion sheds ‘tail’ to escape: consequences and implications of autotomy in scorpions (Buthidae: Ananteris). PLoS One 10(1):e0116639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miller AL, Formanowicz DR (2011) Friend or foe: behavioral responses to conspecifics in the northern scorpion, Paruroctonus boreus (Scorpionida: Vaejovidae). J Ethol 29(2):251–256

    Article  Google Scholar 

  • Moreno-González JA, Hazzi NA (2012) Intraguild predation case: Tityus forcipula Gervais, 1843 (Scorpiones, Buthidae) feeding on Chactas vanbenedeni Gervais, 1843 (Scorpiones, Chactidae) in Colombia. Rev Iber Aracnol 20:117–120

  • Nime MF, Casanoves F, Vrech DE, Mattoni CI (2013) Relationship between environmental variables and surface activity of scorpions in the Arid Chaco ecoregion of Argentina. Invertebr Biol 132(2):145–155

    Article  Google Scholar 

  • Nisani Z, Honaker A, Jenne V, Loya F, Moon H (2018) Evidence of airborne chemoreception in the scorpion Paruroctonus marksi (Scorpiones: Vaejovidae). J Arachnol 46(1):40–44

    Article  Google Scholar 

  • Okuyama T (2002) The role of antipredator behavior in an experimental community of jumping spiders with intraguild predation. Popul Ecol 44(2):121–125

    Article  Google Scholar 

  • Olivero PA, Mattoni CI, Peretti AV (2017) Differences in mating behavior between two allopatric populations of a Neotropical scorpion. Zoology 123:71–78

    Article  PubMed  Google Scholar 

  • Pears JB, Emberts Z, Bateman PW (2018) The scent of danger: the impact of predator chemical cues on emergence from refuge and willingness to autotomize limbs in the house cricket (Acheta domesticus). J Insect Behav 31:416–426

    Article  Google Scholar 

  • Persons MH, Walker SE, Rypstra AL, Marshall SD (2001) Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae). Anim Behav 61(1):43–51

    Article  PubMed  Google Scholar 

  • Persons MH, Walker SE, Rypstra AL (2002) Fitness costs and benefits of antipredator behavior mediated by chemotactile cues in the wolf spider Pardosa milvina (Araneae: Lycosidae). Behav Ecol 13(3):386–392

    Article  Google Scholar 

  • Polis GA, McCormick SJ (1986) Patterns of resource use and age structure among species of desert scorpion. J Anim Ecol 55:59–73

    Article  Google Scholar 

  • Polis GA, McCormick SJ (1987) Intraguild predation and competition among desert scorpions. Ecology 68(2):332–343

    Article  Google Scholar 

  • Polis GA, Sissom WD, McCormick SJ (1981) Predators of scorpions: field data and a review. J Arid Environ 4:309–326

    Article  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20(1):297–330

    Article  Google Scholar 

  • Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions. Ecology 88(11):2744–2751

    Article  PubMed  Google Scholar 

  • Queiroz M, Gasnier TR (2017) Strong negative effect of diurnal rainfall on nocturnal activity of a wandering spider in Central Amazonia. Rev Biol Trop 65(3):1152–1160

    Article  Google Scholar 

  • Riddle WA, Crawford CS, Zeitone AM (1976) Patterns of hemolymph osmoregulation in three desert arthropods. J Comp Physiol 112(3):295–305

    Article  Google Scholar 

  • RStudio Team (2019) RStudio: integrated development for R. RStudio, Inc., Boston. Available from: <http://www.rstudio.com/>. Accessed: 01 Feb 2019

  • Ryan D, Cantrell RS (2015) Avoidance behavior in intraguild predation communities: a cross-diffusion model. Discrete Cont Dyn S 35:1641–1663

    Article  Google Scholar 

  • Sampaio EVDSB, Dall’Olio A, Nunes KS, Lemos EEP (1993) A model of litterfall, litter layer losses and mass transfer in a humid tropical forest at Pernambuco, Brazil. J Trop Ecol 9(3):291–301

    Article  Google Scholar 

  • Sánchez-Piñero F, Urbano-Tenorio F (2016) Watch out for your neighbor: climbing onto shrubs is related to risk of cannibalism in the scorpion Buthus cf. occitanus. PloS One 11(9):e0161747

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santos GCSG, Dionisio-da-Silva W, Souza-Alves JP, Albuquerque CMR, Lira AFA (2018) Random or clumped: how litter dwelling scorpions are distributed in a fragment of Brazilian Atlantic forest. Eur J Entomol 115:445–449

    Article  Google Scholar 

  • Scharf I, Nulman E, Ovadia O, Bouskila A (2006) Efficiency evaluation of two competing foraging modes under different conditions. Am Nat 168(3):350–357

    Article  PubMed  Google Scholar 

  • Schmidt JM, Rypstra AL (2010) Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters. Oecologia 164(4):899–910

    Article  PubMed  Google Scholar 

  • Schmidt JM, Sebastian P, Wilder SM, Rypstra AL (2012) The nutritional content of prey affects the foraging of a generalist arthropod predator. PLoS One 7(11):e49223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt JM, Crist TO, Wrinn K, Rypstra AL (2014) Predator interference alters foraging behavior of a generalist predatory arthropod. Oecologia 175(2):501–508

    Article  PubMed  Google Scholar 

  • Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319(5865):952–954

    Article  CAS  PubMed  Google Scholar 

  • Sharpe PB, Van Horne B (1998) Influence of habitat on behavior of Townsend’s ground squirrels (Spermophilus townsendii). J Mammal 79(3):906–918

    Article  Google Scholar 

  • Snyder WE, Wise DH (2000) Antipredator behavior of spotted cucumber beetles (Coleoptera: Chrysomelidae) in response to predators that pose varying risks. Environ Entomol 29(1):35–42

    Article  Google Scholar 

  • Stockmann R (2015) Introduction to scorpion biology and ecology. In: Gopalakrishnakone P (ed), Scorpion Venoms, Springer Netherlands, pp.25–59

  • Stoks R, Block MD, Slos S, Doorslaer WV, Rolff J (2006) Time constraints mediate predator-induced plasticity in immune function, condition, and life history. Ecology 87(4):809–815

    Article  PubMed  Google Scholar 

  • Stouffer DB, Bascompte J (2010) Understanding food-web persistence from local to global scales. Ecol Lett 13(2):154–161

    Article  PubMed  Google Scholar 

  • Tchabovsky AV, Krasnov B, Khokhlova IS, Shenbrot GI (2001) The effect of vegetation cover on vigilance and foraging tactics in the fat sand rat Psammomys obesus. J Ethol 19(2):105–113

    Article  Google Scholar 

  • Tobler I, Stalder J (1988) Rest in the scorpion—a sleep-like state? J Comp Physiol A 163(2):227–235

    Article  Google Scholar 

  • Toolson EC, Hadley NF (1977) Cuticular permeability and epicuticular lipid composition in two Arizona vejovid scorpions. Physiol Zool 50(4):323–330

    Article  CAS  Google Scholar 

  • Urbani P, Ramos-Jiliberto R (2010) Adaptive prey behavior and the dynamics of intraguild predation systems. Ecol Model 221(22):2628–2633

    Article  Google Scholar 

  • Webber MM, Gibbs AG, Rodríguez-Robles JA (2015) Hot and not-so-hot females: reproductive state and thermal preferences of female Arizona Bark Scorpions (Centruroides sculpturatus). J Evol Biol 28(2):368–375

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson EB, Grabowski JH, Sherwood GD, Yund PO (2015) Influence of predator identity on the strength of predator avoidance responses in lobsters. J Exp Mar Biol Ecol 465:107–112

    Article  Google Scholar 

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Acknowledgments

We are also very grateful to the military command of the CIMNC for permission to use the area for our study and to Divisão de Transportes da Universidade Federal de Pernambuco for all technical support.

Funding

This work was supported by the Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE) (grant number: APQ-0.437-2.04/15) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a financial support to CMR Albuquerque (grant number: 307759/2015-6). We are grateful to Fundação de Apoio à Pesquisa do Estado da Paraíba (FAPESQ) for granting a doctoral scholarship to W. Dionisio-da-Silva (grant number: 519/18) and to Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for postdoctoral scholarship (BFP-0010-2.05/19) to A.F.A. Lira.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Biológicas, Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, João Pessoa, PB, CEP 58051-090, Brazil

    Welton Dionisio-da-Silva

  2. Programa de Pós-graduação em Biologia Animal, Departamento de Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, CEP 50670-420, Brazil

    Welton Dionisio-da-Silva & Cleide Maria Ribeiro de Albuquerque

  3. Programa de Pós-Graduação em Ciência Animal Tropical, Departamento de Morfologia e Fisiologia Animal, Universidade Federal Rural de Pernambuco, Recife, PE, CEP 52171-900, Brazil

    André Felipe de Araujo Lira

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  1. Welton Dionisio-da-Silva
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Correspondence to Welton Dionisio-da-Silva.

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This article did not contain any studies with human participants and also did not involve endangered or protected species. It was approved by Sistema de Autorização e Informação em Biodiversidade/Instituto Chico Mendes de Conservação da Biodiversidade (SISBIO/ICMBIO no. 36336-1) and complied with Brazilian law. All procedures of this work were determined to assure the animals’ welfare. Animal collection and handling was conducted with the use of tweezers without harming the animals. The experiments were conducted with only healthy animals. Water supply and shelters were made available for the animals during the experimental trials, and food was also made available during their rearing. Application of non-toxic paint markings on the individuals during the experiments is a minimally invasive technique. The animals were returned to the wild after the study.

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Dionisio-da-Silva, W., de Araujo Lira, A.F. & de Albuquerque, C.M.R. Prey-predator interactions between two intraguild predators modulate their behavioral decisions. acta ethol 22, 195–201 (2019). https://doi.org/10.1007/s10211-019-00326-6

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