Abstract
Predation is a well-known factor that structures rotifer communities. However, the role of protists as predators is relatively understudied. Here, we investigated predatory behavior of Actinosphaerium sp., a freshwater heliozoan, on seven rotifer species. Predators and prey were collected from a local playa; except for Brachionus calyciflorus that served as a naive prey control. Prey included large species (≥ 175 µm mean length: Asplanchna sieboldii, B. calyciflorus, Platyias quadricornis, and Lacinularia flosculosa) and small species (< 175 µm: Cephalodella gibba, Euchlanis dilatata, and Lepadella patella). Four experiments were conducted. (1) Single prey items of varying size and motility. Larger prey types were ~ 1.7 to 3.0 times more likely to be ingested than small prey. No L. flosculosa were ingested, contrary to field observations. No correlation was found between swimming speed and predation risk. (2) Preference tests. Asplanchna sieboldii and B. calyciflorus were favored prey. (3) Growth rate of Actinosphaerium on mixed diets, with and without Asplanchna. Highest population growth of Actinosphaerium was observed in presence of A. sieboldii. (4) Prey defenses. Susceptibility of spined versus unspined B. calyciflorus resulted in no significant difference in predation risk. Thus, size and being mobile (compared to sessility) are the primary risk factors influencing rotifer predation vulnerability.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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References
Almeda, R., H. van Someren Gréve & T. Kiørboe, 2017. Behavior is a major determinant of predation risk in zooplankton. Ecosphere 8(2): e01668. https://doi.org/10.1002/ecs2.1668.
Alvarado-Flores, J., M. A. Arzate-Cárdenas, D. Pérez-Yañez & E. Cejudo, 2022. Environmental stressor induces morphological alterations in zooplankton. Latin American Journal of Aquatic Research 50(1): 1–12. https://doi.org/10.3856/vol50-issue1-fulltext-2774.
Balsamo, M., T. Artois, J. P. Smith, M. A. Todaro, L. Guidi, B. S. Leander & N. W. Van Steenkiste, 2020. The curious and neglected soft-bodied meiofauna: Rouphozoa (Gastrotricha and Platyhelminthes). Hydrobiologia 847(12): 2613–2644. https://doi.org/10.1007/s10750-020-04287-x.
Bell, E. M., G. Weithoff & U. Gaedke, 2006. Temporal dynamics and growth of Actinophrys sol (Sarcodina: Heliozoa), the top predator in an extremely acidic lake. Freshwater Biology 51: 1149–1161. https://doi.org/10.1111/j.1365-2427.2006.01561.x.
Bhadra, M., M. Kobayashi, R. Higuchi, L. Chen & T. Suzaki, 2017. Major vault protein of the protozoan Raphidiophrys contractilis has a binding property to β-1,3-glucan and is involved in food capturing. International Journal of New Technology and Research 3(7): 1–7.
Buonanno, F., T. Harumoto & C. Ortenzi, 2013. The defensive function of trichocysts in Paramecium tetraurelia against metazoan predators compared with the chemical defense of two species of toxin-containing ciliates. Zoological Science 30(4): 255–261. https://doi.org/10.2108/zsj.30.255.
Buonanno, F., A. Anesi, G. Di Giuseppe, G. Guella & C. Ortenzi, 2017. Chemical defense by erythrolactones in the euryhaline ciliated protist, Pseudokeronopsis erythrina. Zoological Science 34(1): 42–51. https://doi.org/10.2108/zs160123.
Buonanno, F., E. Catalani, D. Cervia, C. Cimarelli, E. Marcantoni & C. Ortenzi, 2020. Natural function and structural modification of climacostol, a ciliate secondary metabolite. Microorganisms 8(6): 809. https://doi.org/10.3390/microorganisms8060809.
Buskey, E. J., J. R. Strickler, C. J. Bradley, D. K. Hartline & P. H. Lenz, 2017. Escapes in copepods: comparison between myelinate and amyelinate species. Journal of Experimental Biology 220(5): 754–758. https://doi.org/10.1242/jeb.148304.
Chin, N. E., T. C. Wu, J. M. O’Toole, K. Xu, T. Hata & M. A. R. Koehl, 2022. Formation of multicellular colonies by choanoflagellates increases susceptibility to capture by amoeboid predators. Journal of Eukaryotic Microbiology. https://doi.org/10.1111/jeu.1296.
Diéguez, M. & E. Balseiro, 1998. Colony size in Conochilus hippocrepis: defensive adaptation to predator size. Hydrobiologia 387(388): 421–425. https://doi.org/10.1023/A:1017042610913.
Esteban, G. F. & T. M. Fenchel, 2020. Feeding. In Esteban, G. F. & T. M. Fenchel (eds), Ecology of Protozoa. Springer, Cham, Switzerland: 33–54.
Feike, M. & R. Heerkloss, 2009. Does Eurytemora affinis (Copepoda) control the population growth of Keratella cochlearis (Rotifera) in the brackish water Darß-Zingst Lagoon (southern Baltic Sea)? Journal of Plankton Research 31(5): 571–576. https://doi.org/10.1093/plankt/fbp004.
Felix, A., M. E. Stevens & R. L. Wallace, 1995. Unpalatability of a colonial rotifer, Sinantherina socialis, to small zooplanktivorous fishes. Invertebrate Biology 114: 139–144. https://doi.org/10.2307/3226885.
Garcia, M. A., 2004. The asexual life history of the colonial rotifer, Sinantherina socialis (Linnaeus). Department of Biology and Evolutionary Biology. Doctoral Dissertation, Yale University, New Haven: 129.
Garza-Mouriño, G., M. Silva-Briano, S. Nandini, S. S. S. Sarma & M. E. Castellanos-Páez, 2005. Morphological and morphometric variations of selected rotifer species in response to predation: a seasonal study of selected brachionid species ftom Lake Xochimilco (Mexico). Hydrobiologia 546: 169–179. https://doi.org/10.1007/s10750-005-4114-5.
Gilbert, J. J., 1966. Rotifer ecology and embryological induction. Science 151: 1234–1237. https://doi.org/10.1126/science.151.3715.123.
Gilbert, J. J., 1967. Asplanchna and postero-lateral spine production in Brachionus calyciflorus. Archiv Für Hydrobiologie 64(1): 1–62.
Gilbert, J. J., 1977. Defenses of males against cannibalism in the rotifer Asplanchna: size, shape, and failure to elicit tactile feeding response. Ecology 58(5): 1128–1135. https://doi.org/10.2307/1936933.
Gilbert, J. J., 1980a. Further observations on developmental polymorphism and its evolution in the rotifer Brachionus calyciflorus. Freshwater Biology 10(3): 281–294. https://doi.org/10.1111/j.1365-2427.1980.tb01202.x.
Gilbert, J. J., 1980b. Observations on the susceptibility of some protists and rotifers to predation by Asplanchna girodi. Hydrobiologia 73: 87–91. https://doi.org/10.1007/978-94-009-9209-2_17.
Gilbert, J. J., 1985. Escape response of the rotifer Polyarthra: a high-speed cinematographic analysis. Oecologia 66: 322–331. https://doi.org/10.1007/BF00378293.
Gilbert, J. J., 2009. Predator-specific inducible defenses in the rotifer Keratella tropica. Freshwater Biology 54: 1933–1946. https://doi.org/10.1111/j.1365-2427.2009.02246.x.
Gilbert, J. J., 2011. Induction of different defences by two enemies in the rotifer Keratella tropica: response priority and sensitivity to enemy density. Freshwater Biology 56(5): 926–938. https://doi.org/10.1111/j.1365-2427.2010.02538.x.
Gilbert, J. J., 2017. Spine development in two taxa of Brachionus calyciflorus from Lake Littra, Australia: constitutive and induced defenses against Asplanchna. Journal of Plankton Research 39(6): 962–971. https://doi.org/10.1093/plankt/fbx048.
Gilbert, J. J., 2018. Morphological variation and its significance in a polymorphic rotifer: environmental, endogenous, and genetic controls. BioScience 68(3): 169–181. https://doi.org/10.1093/biosci/bix162.
Gilbert, J. J., 2019. Attachment behavior in the rotifer Brachionus rubens: induction by Asplanchna and effect on sexual reproduction. Hydrobiologia 844: 9–20. https://doi.org/10.1007/s10750-018-3805-7.
Gilbert, J. J. & C. W. Burns, 2000. Day and night vertical distributions of Conochilus and other zooplankton in a New Zealand reservior. Verhandlungen Internationale Vereinigung Limnologie 27: 1909–1914.
Gilbert, J. J. & J. L. Confer, 1986. Gigantism and the potential for interference competition in the rotifer genus Asplanchna. Oecologia 70(4): 549–554. https://doi.org/10.1007/BF00379902.
Gilbert, J. J. & M. C. Diéguez, 2010. Low crowding threshold for induction of sexual reproduction and diapause in a Patagonian rotifer. Freshwater Biology 55: 1705–1718. https://doi.org/10.1111/j.1365-2427.2010.02405.x.
Gilbert, J. J. & K. L. Kirk, 1988. Escape response of the rotifer Keratella: description, stimulation, fluid dynamics, and ecological significance. Limnology and Oceanography 33(6): 1440–1450. https://doi.org/10.4319/lo.1988.33.6part2.1440.
Gilbert, J. J. & J. R. Litton, 1978. Sexual reproduction in the rotifer Asplanchna girodi: effects of tocopherol and population density. Journal of Experimental Zoology 204(1): 113–121. https://doi.org/10.1002/jez.1402040110.
Gilbert, J. J. & R. W. Stemberger, 1984. Asplanchna-induced polymorphism in the rotifer Keratella slacki. Limnology and Oceanography 29(6): 1309–1316. https://doi.org/10.4319/lo.1984.29.6.1309.
Gilbert, J. J. & G. A. Thompson Jr., 1968. Alpha tocopherol control of sexuality and polymorphism in the rotifer Asplanchna. Science 159: 734–736. https://doi.org/10.1126/science.159.3816.734.
Green, J., 2007. Morphological variation of Keratella cochlearis (Gosse) in Myanmar (Burma) in relation to zooplankton community structure. Hydrobiologia 593(1): 5–12. https://doi.org/10.1007/s10750-007-9072-7.
Green, J. D. & R. J. Shiel, 1992. A dissection method for determining the gut contents of calanoid copepods. Transactions of the Royal Society of South Australia 116(4): 129–132.
Gunter, D. D. & L. A. Knight Jr., 1978. Observations of the rotifer Sinantherina semibullata (Thorpe) from Ross Barnett reservoir. Mississippi. Egyptian Journal of Microbiology 13(12): 99–106.
Hampton, S. E. & J. J. Gilbert, 2001. Observations of insect predation on rotifers. Hydrobiologia 446(447): 115–121. https://doi.org/10.1023/A:1017543121353.
Hampton, S. E., J. J. Gilbert & C. W. Burns, 2000. Direct and indirect effects of juvenile Buenoa macrotibialis (Hemiptera: Notonectidae) on the zooplankton of a shallow pond. Limnology and Oceanography 45(4): 1006–1012. https://doi.org/10.4319/lo.2000.45.4.1006.
Havens, K. E., 1990. Chaoborus predation and zooplankton community structure in a rotifer-dominated lake. Hydrobiologia 198(1): 215–226. https://doi.org/10.1007/BF00048636.
Hershey, A. E. & S. I. Dodson, 1987. Predator avoidance by Cricotopus: cyclomorphosis and the importance of being big and hairy. Ecology 68(4): 913–920. https://doi.org/10.2307/1938362.
Herzog, Q., C. Tittgen & C. Laforsch, 2016. Predator-specific reversibility of morphological defenses in Daphnia barbata. Journal of Plankton Research 38(4): 771–780. https://doi.org/10.1093/plankt/fbw045.
Hochberg, R. & A. Ablak Gurbuz, 2007. Functional morphology of somatic muscles and anterolateral setae in Filinia novaezealandiae Shiel and Sanoamuang, 1993 (Rotifera). Zoologischer Anzeiger 246: 11–22. https://doi.org/10.1016/j.jcz.2006.10.002.
Hochberg, R., A. Hochberg & C. Chan, 2015. Ultrastructure of the rotifer integument: peculiarities of Sinantherina socialis (Monogononta: Gnesiotrocha). Invertebrate Biology 134(3): 181–188. https://doi.org/10.1111/ivb.12085.
Jacobs, J., 1974. Quantitative measurement of food selection. Oecologia 14(4): 413–417. https://doi.org/10.1007/BF00384581.
Jara, F. G. & M. G. Perotti, 2010. Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644(1): 313–324. https://doi.org/10.1007/s10750-010-0196-9.
Järvenpää, M. & K. Lindström, 2004. Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proceedings of the Royal Society of London Series b: Biological Sciences 271: 2361–2365. https://doi.org/10.1098/rspb.2004.2870.
Jezkova, I., R. Ortells, J. Montero-Pau & M. Serra, 2022. Insight into incipient reproductive isolation in diverging populations of Brachionus plicatilis rotifer. Hydrobiologia 849(15): 3299–3311. https://doi.org/10.1007/s10750-022-04927-4.
Kerfoot, W. C., 1982. A question of taste: crypsis and warning coloration in freshwater zooplankton communities. Ecology 63(2): 538–554. https://doi.org/10.2307/1938969.
Kerfoot, W. C., D. L. J. Kellogg & J. R. Strickler, 1980. Visual observations of live zooplankters: evasion, escape, and chemical defenses. In Kerfoot, W. C. (ed.), Evolution and Ecology of Zooplankton Communities. The University Press of New England, Hanover: 10–27.
Kossova, A. A., 1979. Contraction of Sinantherina semibullata (Monimotrochida, Flosculariidae) as a defense reaction against eating out. Zoologichekii Zhurnal 58(11): 1728–1729 (in Russian, with English summary).
Koste, W., 1981. Zur Morphologie, Systematik und Ökologie von neuen monogononten Rädertieren (Rotatoria) aus dem Überschwemmungsgebiet des Magela Creek in der Alligator-River-Region Australiens, N.T. Teil 1. Osnabrücker Naturwissenschaftliche Mitteilungen 8: 97–126.
Kulmer, W. E., J. Jorge, P. M. Kim, N. Iftekhar & M. A. R. Koehl, 2020. Does formation of multicellular colonies by choanoflagellates affect their susceptibility to capture by passive protozoan predators? Journal of Eukaryotic Microbiology 67(5): 555–565. https://doi.org/10.1111/jeu.12808.
Kumar, R., S. Kumari, A. Malika, A. P. Sharma & H. U. Dahms, 2022. Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod. Scientific Reports 12(1): 22631. https://doi.org/10.1038/s41598-022-26004-5.
Lair, N., H. Taleb & P. Reyes-Marchant, 1996. Horizontal distribution of the rotifer plankton of Lake Aydat (France). Aquatic Sciences 58(3): 253–268. https://doi.org/10.1007/BF00877512.
Li, Y., R. Wang, H. Su, J. Wang, P. Xie & F. Chen, 2022. Eutrophication and predation mediate zooplankton diversity and network structure. Limnology and Oceanography 67: S133–S145. https://doi.org/10.1002/lno.11957.
Lou, Y. & H. Nie, 2022. Global dynamics of a generalist predator–prey model in open advective environments. Journal of Mathematical Biology 84(6): 46. https://doi.org/10.1007/s00285-022-01756-w.
Lynch, M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnology and Oceanography 24(2): 253–272. https://doi.org/10.4319/lo.1979.24.2.0253.
MacArthur, R. H. & E. R. Pianka, 1966. On optimal use of a patchy environment. The American Naturalist 100(916): 603–609. https://doi.org/10.1086/282454.
Meksuwan, P., P. Pholpunthin, E. J. Walsh, H. Segers & R. L. Wallace, 2014. Nestedness in sessile and periphytic rotifer communities: a meta-analysis. International Review of Hydrobiology 99(1–2): 48–57. https://doi.org/10.1002/iroh.201301703.
Mikrjukov, K. A. & D. J. Patterson, 2001. Taxonomy and phylogeny of Heliozoa. III. Actinophryids. Acta Protozoologica 40: 3–25.
Moore, M. V. & J. J. Gilbert, 1987. Age-specific Chaoborus predation on rotifer prey. Freshwater Biology 17(2): 223–236. https://doi.org/10.1111/j.1365-2427.1987.tb01044.x.
Morgan, A. M., T. V. Royer, M. B. David & L. E. Gentry, 2006. Relationships among nutrients, chlorophyll- a, and dissolved oxygen in agricultural streams in Illinois. Journal of Environmental Quality 35(4): 1110–1117. https://doi.org/10.2134/jeq2005.0433.
Obertegger, U., A. Cieplinski, M. Raatz & P. Colangeli, 2018. Switching between swimming states in rotifers—case study Keratella cochlearis. Marine and Freshwater Behaviour and Physiology 51(3): 159–173. https://doi.org/10.1080/10236244.2018.1503541.
Parry, V., U. E. Schlägel, R. Tiedemann & G. Weithoff, 2022. Behavioural responses of defended and undefended prey to their predator—A case study of Rotifera. Biology 11(8): 1217. https://doi.org/10.3390/biology11081217.
Parysek, M. & B. Pietrzak, 2020. Weak swimming response of a bdelloid rotifer to chemical cues of a native copepod predator. Journal of Ethology 39(1): 135–139. https://doi.org/10.1007/s10164-020-00676-w.
Pourriot, R., 1974. Relations prédature-poie chex les rotifères: influence du prédature (Asplanchna brightwelli) sur la morphologie de la proie (Brachionus bidentata). Annales D’hydrobiologie 5(1): 43–55.
Pusack, T. J., J. W. White, H. G. Tillotson, D. L. Kimbro & C. D. Stallings, 2018. Size-dependent predation and intraspecific inhibition of an estuarine snail feeding on oysters. Journal of Experimental Marine Biology and Ecology 501: 74–82. https://doi.org/10.1016/j.jembe.2018.01.005.
Pyke, G. H., 1984. Optimal Foraging Theory: a critical review. Annual Review of Ecology and Systematics 15: 523–575. https://doi.org/10.1146/annurev.es.15.110184.002515.
R_Core_Team, 2022. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Rico-Martinez, R. & T. W. Snell, 1997. Mating behavior in eight rotifer species: using cross-mating tests to study species boundaries. Hydrobiologia 356: 165–173. https://doi.org/10.1023/A:1003194216467.
Riessen, H. P. & J. J. Gilbert, 2018. Divergent developmental patterns of induced morphological defenses in rotifers and Daphnia: ecological and evolutionary context. Limnology and Oceanography. https://doi.org/10.1002/lno.11058.
Sakaguchi, M., H. Murakami & T. Suzaki, 2001. Involvement of a 40-kDa glycoprotein in food recognition, prey capture, and induction of phagocytosis in the protozoan Actinophrys sol. Protist 152(1): 33–41. https://doi.org/10.1078/1434-4610-00041.
Salt, G. W., 1987. The components of feeding behavior in rotifers. Hydrobiologia 147(1): 271–281. https://doi.org/10.1007/BF00025754.
Santos-Medrano, G. E., R. Rico-Martinez & C. A. Velásquez-Rojas, 2001. Swimming speed and Reynolds numbers of eleven freshwater rotifer species. Hydrobiologia 446(447): 35–38. https://doi.org/10.1023/A:1017512820019.
Santos-Medrano, G. E., D. Robles-Vargas, S. Hernández-Flores & R. Rico-Martínez, 2017. Life table demography of Asplanchna brightwellii Gosse, 1850 fed with five different prey items. Hydrobiologia 796(1): 169–179. https://doi.org/10.1007/s10750-016-3069-z.
Sarma, S. S. S. & S. Nandini, 2007. Small prey size offers immunity to predation: a case study on two species of Asplanchna and three brachionid prey (Rotifera). Hydrobiologia 593: 67–76. https://doi.org/10.1007/s10750-007-9069-2.
Sarma, S. S. S., R. A. Lara Resendiz & S. Nandini, 2011. Morphometric and demographic responses of brachionid prey (Brachionus calyciflorus Pallas and Plationus macracanthus (Daday) in the presence of different densities of the predator Asplanchna brightwellii (Rotifera: Asplanchnidae). Hydrobiologia 622: 179–187. https://doi.org/10.1007/s10750-010-0494-2.
Smith, G., 1903. Actinosphaerium eichorni: a biometrical study in the mass relations of nucleus and cytoplasm. Biometrika 2(3): 241–254. https://doi.org/10.2307/2331600.
Snell, T. W. & P. D. Morris, 1993. Sexual communication in copepods and rotifers. Hydrobiologia 255(256): 109–116. https://doi.org/10.1007/BF00025828.
Snell, T. W. & R. Rico-Martinez, 1996. Characteristics of the mate-recognition pheromone in Brachionus plicatilis (Rotifera). Marine and Freshwater Behaviour and Physiology 27(2–3): 143–151. https://doi.org/10.1080/10236249609378960.
Snell, T. W., R. Rico-Martinez, L. N. Kelly & T. E. Battle, 1995. Identification of a sex pheromone from a rotifer. Marine Biology 123: 347–353. https://doi.org/10.1007/BF00353626.
Snell, T. W., R. K. Johnston & A. B. Matthews, 2018. Utilizing Brachionus biodiversity in marine finfish larviculture. Hydrobiologia 844(1): 149–162. https://doi.org/10.1007/s10750-018-3776-8.
Snyder, W. E. & D. H. Wise, 2001. Contrasting trophic cascades generated by a community of generalist predators. Ecology 82(6): 1571–1583. https://doi.org/10.1890/0012-9658(2001)082[1571:CTCGBA]2.0.CO;2.
Soto, C. S. & S. S. S. Sarma, 2009. Morphological changes in Lecane stokesii (Pell, 1890) (Rotifera: Lecanidae) induced by allelochemicals from the predator Asplanchopus multiceps (Schrank, 1793). Allelopthy Journal 23(2): 215–222.
Stemberger, R. S., 1981. A general approach to the culture of planktonic rotifers. Canadian Journal of Fisheries and Aquatic Sciences 38: 721–724. https://doi.org/10.1139/cjfas-2015-0076.
Stemberger, R. S., 1985. Prey selection by the copepod Diacyclops thomasi. Oecologia 65(4): 492–497. https://doi.org/10.1007/BF00379662.
Stemberger, R. S. & J. J. Gilbert, 1984. Spine development in the rotifer Keratella cochlearis: induction by cyclopoid copepods and Asplanchna. Freshwater Biology 14: 639–647. https://doi.org/10.1111/j.1365-2427.1984.tb00183.x.
Stemberger, R. S. & J. J. Gilbert, 1987a. Multiple-species induction of morphological defenses in the rotifer Keratella testudo. Ecology 68: 370–378. https://doi.org/10.2307/1939268.
Stemberger, R. S. & J. J. Gilbert, 1987b. Defenses of planktonic rotifers against predators. In Kerfoot, W. C. & A. Sih (eds), Predation: Direct and Indirect Impacts on Aquatic Communities. University Press of New England, Hanover: 227–239.
Stenson, J. A. E., 1982. Fish impact on rotifer community structure. Hydrobiologia 87(1): 57–64. https://doi.org/10.1007/BF00016662.
Stenson, J. A. E., 1987. Variation in capsule size of Holopedium gibberum (Zaddach): a response to invertebrate predation. Ecology 68(4): 928–934. https://doi.org/10.2307/1938364.
Strong, D. R., 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73(3): 747–754. https://doi.org/10.2307/1940154.
Wallace, R. L., 1980. Ecology of sessile rotifers. Hydrobiologia 73: 181–193. https://doi.org/10.1007/978-94-009-9209-2_31.
Wallace, R. L., 1987. Coloniality in the phylum Rotifera. Hydrobiologia 147: 141–155. https://doi.org/10.1007/978-94-009-4059-8_20.
Wallace, R. L. & H. A. Smith, 2009. Rotifera. In Likens, G. E. (ed.), Encyclopedia of Inland Waters, Vol. 3. Elsevier, Oxford: 689–703.
Wallace, R. L., T. W. Snell, C. Ricci & T. Nogrady, 2006. Rotifera: Biology, Ecology and Systematics, 2 ed., Vol. 1. Backhuys Publishers, Leiden.
Wallace, R. L., T. W. Snell & H. A. Smith, 2015. Phylum Rotifera. In Thorp, J. H. & D. C. Rogers (eds), Thorp and Covich’s Freshwater Invertebrates, Ecology and General Biology. Vol. I. Elsevier, Waltham: 225–271.
Walsh, E. J., 1995. Habitat-specific predation susceptibilities of a littoral rotifer to two invertebrate predators. Hydrobiologia 313(314): 205–211. https://doi.org/10.1007/BF00025952.
Walsh, E. J., M. Salazar, J. Remirez, O. Moldes & R. L. Wallace, 2006. Predation by invertebrate predators on the colonial rotifer Sinantherina socialis. Invertebrate Biology 125: 325–335. https://doi.org/10.1111/j.1744-7410.2006.00064.x.
Weithoff, G. & E. M. Bell, 2022. Complex trophic Interactions in an acidophilic microbial community. Microorganisms 10(7): 1340. https://doi.org/10.3390/microorganisms10071340.
White, T. E., T. Latty & K. D. L. Umbers, 2022. The exploitation of sexual signals by predators: a meta-analysis. Proceedings of the Royal Society B: Biological Sciences 289: 20220444. https://doi.org/10.1098/rspb.2022.0444.
Williamson, C. E., 1983. Invertebrate predation on planktonic rotifers. Hydrobiologia 104: 385–396. https://doi.org/10.1007/BF00045996.
Williamson, C. E., 1987. Predator–prey interactions between omnivorous diaptomid copepods and rotifers: the role of prey morphology and behavior. Limnology and Oceanography 32(1): 167–177. https://doi.org/10.4319/lo.1987.32.1.0167.
Williamson, C. E. & R. E. Magnien, 1982. Diel vertical migration in Mesocyclops edax: implications for predation rate estimates. Journal of Plankton Research 4(2): 329–339. https://doi.org/10.1093/plankt/4.2.329.
Yin, X., W. Jin, Y. Zhou, P. Wang & W. Zhao, 2017. Hidden defensive morphology in rotifers: benefits, costs, and fitness consequences. Scientific Reports 7(1): 4488. https://doi.org/10.1038/s41598-017-04809-z.
Zhang, H., C. Brönmark & L.-A. Hansson, 2017. Predator ontogeny affects expression of inducible defense morphology in rotifers. Ecology 98(10): 2499–2505. https://doi.org/10.1002/ecy.1957.
Zhang, H., Y. He, L. He, K. Zhao, J. García Molinos, L. A. Hansson & J. Xu, 2022. Plasticity in rotifer morphology induced by conflicting threats from multiple predators. Freshwater Biology 67(3): 498–507. https://doi.org/10.1111/fwb.13857.
Acknowledgements
We thank Patrick D. Brown and the students in the Walsh laboratory for field assistance. This project was funded in part by CONACYT 2021-000021-01EXTF-00067 (ASSA) and the National Science Foundation (DEB 2051704 (EJW) and DEB 2051710 (RLW)).
Funding
This project was funded in part by several agencies including the National Science Foundation: DEB 2051704 (EJW); DEB 2051710 (RLW), the Ripon College SOAR program (RLW), and CONACYT 2021-000021-01EXTF-00067 (ASSA).
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Conceptualization, EJW, ASA; validation, EJW, ASA; formal analysis, ASA; investigation, EJW, ASA; resources, EJW, RLW; data curation, EJW, ASA; photomicrographs, ASA; writing—original draft preparation, ASA, EJW, RLW; writing, reviewing, and editing, ASA, EJW, RLW; project administration, EJW; funding acquisition, EJW, RLW. All authors have read and agreed to the published version of the manuscript.
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The authors have no conflicts of interest/competing interests. The sponsors had no role in the design, execution, interpretation, or writing of the study.
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Heliozoans and rotifers from Hueco Tanks State Park and Historic Site were collected under permit 07-21 issued to E.J. Walsh.
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Sanchez-Avila, A.S., Wallace, R.L. & Walsh, E.J. Motility and size of rotifers as risk factors for being consumed by the passive protistan predator Actinosphaerium sp.. Hydrobiologia 851, 3109–3123 (2024). https://doi.org/10.1007/s10750-023-05260-0
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DOI: https://doi.org/10.1007/s10750-023-05260-0