Beyond Body Mass: How Prey Traits Improve Predictions of Functional Response Parameters

Beyond Body Mass: How Prey Traits Improve Predictions of Functional Response Parameters

Beyond body mass: how prey traits improve predictions of functional response parameters

Ryan M. Kalinoski1,2and John P DeLong3,4

1College of Arts & Sciences, University of St. Francis, Joliet, IL 60453

2Current address: Graduate School of Biological Sciences, Eastern Illinois University, Charleston, IL 61920

3School of Biological Sciences, University of Nebraska – Lincoln, Lincoln, NE 68588

4Corresponding authors: .

Electronic Supplementary Materials

Figure S1. Functional response data and fits for each of 50 predator prey interaction found in the literature search. Each plot shows feeding rate against prey density. Data sets are presented from 1 to 50 from top left to bottom right and conform to the data set numbering of Table S2.

C Users John Documents Projects Cyclops functional responses FigureS2 all data tif

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Table S1. Sources for functional response data, predator and prey species names, and additional sources used to identify body mass of predator and prey species. An X indicates that mass was found in the same source as the functional response.

Source / Predator Species / Prey Species / Predator Mass / Prey Mass
Brandl (1998) / Cyclops vicinus / Bosmina longirostris
Polyarthra dolichoptera
Keratella cochlearis / George (1976) / Michaloudi (2005);González et al. (2008)
Enríquez-García et al. (2013) / Acanthocyclops americanus / Acanthocyclops americanus nauplii
Brachionus havanaensis
Moina micrura / García et al. (2011) / González et al. (2008)
Krylov (1988) / Megacyclops gigas / Cyclopoid Copepodites
Daphnia galeata
Copepd nauplii
Ceriodaphnia pulchella / X / X
Kumar and Ramakrishna Rao (2003) / Mesocyclops thermocyclopoides / Anopheles stephensi - instar I
Culex quinquefasciatus - instar I
Anopheles stephensi - instar IV
Culex quinquefasciatus - instar IV / Kumar and Rao (1999) / Bradshaw (1983)
Marković et al. (2008) / Diacyclops bicuspidatus / Panagrolaimus sp. / X / X
Novich et al. (2014) / Orthocyclops modestus / Urocentrum turbo / X / X
Plaβmann et al. (1997) / Cyclops vicinus / Synchaeta spp. (S.oblonga and S.pectinata)
Polyarthra spp. (P.vulgaris and P.dolichoptera) / George (1976); Hwang et al. (2009) / Michaloudi (2005)
Rabette et al. (1998) / Cyclops vicinus / Cyclidium sp.
Tetrahymena corlissi / (George 1976) / X
Roche (1990) / Acanthocyclops robustus / Synchaeta pectinata
Daphnia hyalina
Synchaeta kitina
Brachionus calyciflorus
Keratella cochlearis / González et al. (2008) / Baudouin and Ravera (1972); Bowen and Johannsson (2011); González et al. (2008); Michaloudi (2005)
Sarma et al. (2013) / Mesocyclops pehpeiensis / Brachionus rubens / Hwang et al. (2009) / X
Van Den Bosch and Santer (1993) / Cyclops abyssorum / Brachionus rubens
Daphnia hyalin (small size)
Daphnia hyalin (medium size)
Daphnia hyalin (large size)
Cyclops abyssorum nauplii stage 2_3_4
Cyclops abyssorum nauplii stage 4_5_6
Cyclops abyssorum copodites stage I
Cyclops abyssorum copodites stage II
Calanoid Nauplii / Jurgens et al. (1997); Manca et al. (1999) / Baudouin and Ravera (1972);Manca et al. (1999);Miller et al. (1977); Sarma et al. (2013)
Wickham (1995) / Cyclops kolensis
Cyclops abyssorum / Askenasia volvox
Halteria grandinella
Strobilidium velox
Stokesia vernalis
Coleps hirtus / Jurgens et al. (1997)
Manca et al. (1999) / X
Williamson (1984) / Mesocyclops edax / Brachionus calcyiflorus
Asplanchna priodonta / Lawrence et al. (1987) / González et al. (2008); Michaloudi (2005)

References

Baudouin MF, Ravera O (1972) Weight, size and chemical composition of some freshwater zooplankters: Daphnia hyalina (Leydig). Limnol Oceanogr 17:645–649.

Bowen KL, Johannsson OE (2011) Changes in zooplankton biomass in the Bay of Quinte with the arrival of the mussels, Dreissena polymorpha and D. rostiformis bugensis, and the predatory cladoceran, Cercopagis pengoi: 1975 to 2008. Aquat Ecosyst Health Manag 14:44–55. doi: 10.1080/14634988.2011.550528

Bradshaw WE (1983) Estimating biomass of mosquito populations. Environ Entomol 12:779–781. doi: 10.1093/ee/12.3.779

Brandl Z (1998) Feeding strategies of planktonic cyclopoids in lacustrine ecosystems. J Mar Syst 15:87–95. doi: 10.1016/S0924-7963(97)00042-0

Enríquez-García C, Nandini S, Sarma SSS (2013) Feeding behaviour of Acanthocyclops americanus (Marsh) (Copepoda: Cyclopoida). J Nat Hist 47:853–862. doi: 10.1080/00222933.2012.747637

García CE, Nandini S, Sarma SSS (2011) Demographic characteristics of the copepod Acanthocyclops americanus (Sars, 1863) (Copepoda: Cyclopoida) fed mixed algal (Scenedesmus acutus)-rotifer (Brachionus havanaensis) diet. Hydrobiologia 666:59–69. doi: 10.1007/s10750-010-0209-8

George DG (1976) Life cycle and production of Cyclops vicinus in a shallow eutrophic reservoir. Oikos 27:101. doi: 10.2307/3543438

González EJ, Matsumura-Tundisi, Tundisi JG (2008) Size and dry weight of main zooplankton species in Bariri reservoir (SP, Brazil). Braz J Biol 68:69–75. doi: 10.1590/S1519-69842008000100010

Hwang J-S, Kumar R, Kuo C-S (2009) Impacts of predation by the copepod, Mesocyclops pehpeiensis, on life table demographics and population dynamics of four cladoceran species: a comparative laboratory study. Zool Stud 48:738–752.

Jurgens K, H A, H Z (1997) Impact of metazoan and protozoan grazers on bacterial biomass distribution in microcosm experiments. Aquat Microb Ecol 12:131–138. doi: 10.3354/ame012131

Krylov P (1988) Predation of the freshwater cyclopoid copepod Megacyclops gigas on lake zooplankton: Functional response and prey selection. Arch Hydrobiol Stuttg 113:231–250.

Kumar R, Ramakrishna Rao T (2003) Predation on mosquito larvae by Mesocyclops thermocyclopoides (Copepoda: Cyclopoida) in the presence of alternate prey. Int Rev Hydrobiol 88:570–581. doi: 10.1002/iroh.200310631

Kumar R, Rao TR (1999) Effect of algal food on animal prey consumption rates in the omnivorous copepod, Mesocyclops thermocyclopoides. Int Rev Hydrobiol 84:419–426. doi: 10.1002/iroh.199900035

Lawrence SG, Malley DF, Findlay WJ, et al (1987) Method for estimating dry weight of freshwater planktonic crustaceans from measures of length and shape. Can J Fish Aquat Sci 44:s264–s274. doi: 10.1139/f87-301

Manca M, Comoli P, Lencioni V (1999) Population dynamics and production of crustacean zooplankton in two mountain lakes in the Italian Alps (Lake Paione Superiore and Lake Malghette). J Limnol. doi: 10.4081/jlimnol.1999.25

Marković M, Threis I, Muschiol D, Traunspurger W (2008) Predator-prey relationship between the cyclopoid copepod Diacyclops bicuspidatus and a free-living bacterivorous nematode. Nematology 10:55–62. doi: 10.1163/156854108783360203

Michaloudi E (2005) Dry weights of the zooplankton of Lake Mikri Prespa (Macedonia, Greece).

Miller CB, Johnson JK, Heinle DR (1977) Growth rules in the marine copepod genus Acartia. Limnol Oceanogr 22:326–335. doi: 10.4319/lo.1977.22.2.0326

Novich RA, Erickson EK, Kalinoski RM, DeLong JP (2014) The temperature independence of interaction strength in a sit-and-wait predator. Ecosphere 5:art137. doi: 10.1890/ES14-00216.1

Plaβmann T, Maier G, Stich HB (1997) Predation impact of Cyclops vicinus on the rotifer community in Lake Constance in spring. J Plankton Res 19:1069–1079. doi: 10.1093/plankt/19.8.1069

Rabette C, Thouvenot A, Lair N (1998) Laboratory experiments on trophic relationships and remote detection between two ciliates and Cyclops vicinus vicinus. Hydrobiologia 373-374:157–167. doi: 10.1023/A:1017001725062

Roche K (1990) Prey features affecting ingestion rates by Acanthocyclops robustus (Copepoda: Cyclopoida) on zooplankton. Oecologia 83:76–82. doi: 10.1007/BF00324637

Sarma SSS, Jiménez-Contreras J, Fernández R, et al (2013) Functional responses and feeding rates of Mesocyclops pehpeiensis Hu (Copepoda) fed different diets (rotifers, cladocerans, alga and cyanobacteria). J Nat Hist 47:841–852. doi: 10.1080/00222933.2012.747636

Van Den Bosch F, Santer B (1993) Cannibalism in Cyclops abyssorum. Oikos 67:19–28.

Wickham SA (1995) Cyclops predation on ciliates: species.specific differences and functional responses. J Plankton Res 17:1633–1646. doi: 10.1093/plankt/17.8.1633

Williamson CE (1984) Laboratory and field experiments on the feeding ecology of the cyclopoid copepod, Mesocyclops edax. Freshw Biol 14:575–585. doi: 10.1111/j.1365-2427.1984.tb00177.x

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Table S2. Functional response parameters, predator and prey species and body mass, prey type, temperature, and R2 values for the functional responses fit to the fifty cyclopoid copepod foraging data sets.

Data
set / Predator species / Prey species / Prey type / Hard shell / Predator mass (μg) / Prey mass (μg) / Temp (C) / Area of capture
(mL pred-1 day-1)
(Cis) / Handling time
(day)
(Cis) / R2
1 / Cyclops kolensis / Askenasia volvox / Ciliate / No / 2.75E+01 / 3.35E-02 / 18 / 10.21 ± 1.4 / 0.99
2 / Cyclops kolensis / Halteria grandinella / Ciliate / No / 2.75E+01 / 5.57E-03 / 18 / 3.9 ± 1.67 / 0.86
3 / Cyclops kolensis / Strobilidium velox / Ciliate / No / 2.75E+01 / 6.54E-02 / 18 / 8 ± 7.5 / 0.0000512 ± 0.0000153 / 0.40
4 / Cyclops kolensis / Stokesia vernalis / Ciliate / No / 2.75E+01 / 9.04E-01 / 18 / 9.2 ± 9.1 / 0.00238 ± 0.0015 / 0.38
5 / Cyclops abyssorum / Askenasia volvox / Ciliate / No / 7.41E+01 / 3.35E-02 / 18 / 4.18 ± 0.42 / 0.0137 ± 0.00122 / 0.95
6 / Cyclops abyssorum / Halteria grandinella / Ciliate / No / 7.41E+01 / 5.57E-03 / 18 / 1.6 ± 0.19 / 0.00951 ± 0.0192 / 0.83
7 / Cyclops abyssorum / Strobilidium velox / Ciliate / No / 7.41E+01 / 6.54E-02 / 18 / 33.22 ± 2.62 / 0.228 ± 0.0684 / 0.99
8 / Cyclops abyssorum / Stokesia vernalis / Ciliate / No / 7.41E+01 / 9.04E-01 / 18 / 6.93 ± 4.95 / 0.343 ± 0.0891 / 0.62
9 / Cyclops abyssorum / Coleps hirtus / Ciliate / No / 7.41E+01 / 1.13E-01 / 18 / 8.81 ± 4.12 / 0.69
10 / Cyclops abyssorum / Brachionus rubens / Rotifer / No / 7.41E+01 / 5.23E-01 / 12 / 78.11 ± 38.22 / 0.11 ± 0.0466 / 0.68
11 / Cyclops abyssorum / Daphnia hyalina (small size) / Cladocera / Yes / 7.41E+01 / 6.23E+01 / 12 / 47.2 ± 17.69 / 0.0357 ± 0.0241 / 0.85
12 / Cyclops abyssorum / Daphnia hyalina (medium size) / Cladocera / Yes / 7.41E+01 / 7.97E+01 / 12 / 47.71 ± 19.47 / 0.233 ± 0.196 / 0.62
13 / Cyclops abyssorum / Daphnia hyalina (large size) / Cladocera / Yes / 7.41E+01 / 1.07E+02 / 12 / 2.95 ± 0.54 / 0.000084 ± 0.663 / 0.72
14 / Cyclops abyssorum / Cyclops abyssorum nauplii stage 2_3_4 / Copepod / Yes / 7.41E+01 / 1.80E-02 / 12 / 28.74 ± 8.61 / 0.0196 ± 0.00971 / 0.68
15 / Cyclops abyssorum / Cyclops abyssorum nauplii stage 4_5_6 / Copepod / Yes / 7.41E+01 / 1.80E-02 / 12 / 20.02 ± 2.97 / 0.000624 ± 0.000125 / 0.93
16 / Cyclops abyssorum / Cyclops abyssorum copodites stage I / Copepod / Yes / 7.41E+01 / 1.70E-01 / 12 / 11.58 ± 3.69 / 0.0000857 ± 0.0000111 / 0.70
17 / Cyclops abyssorum / Cyclops abyssorum copodites stage II / Copepod / Yes / 7.41E+01 / 1.70E-01 / 12 / 3.37 ± 1.33 / 0.68
18 / Cyclops abyssorum / Calanoid Nauplii / Copepod / Yes / 7.41E+01 / 5.00E-01 / 12 / 64.1 ± 11.42 / 0.0144 ± 0.00641 / 0.91
19 / Cyclops vicinus / Cyclidium sp. / Ciliate / No / 9.41E+01 / 1.91E-03 / 15 / 168.51 ± 79.33 / 0.87
20 / Cyclops vicinus / Tetrahymena corlissi / Ciliate / No / 9.41E+01 / 2.47E-02 / 15 / 272.07 ± 63.06 / 0.00178 ± 0.000276 / 0.98
21 / Cyclops vicinus / Bosmina longirostris / Cladocera / Yes / 9.41E+01 / 4.30E+00 / 2.48 ± 0.18 / 0.0239 ± 0.00576 / 0.91
22 / Cyclops vicinus / Polyarthra dolichoptera / Rotifer / No / 9.41E+01 / 4.50E-01 / 8.61 ± 1.45 / 0.0614 ± 0.0328 / 0.94
23 / Cyclops vicinus / Keratella cochlearis / Rotifer / No / 9.41E+01 / 2.50E-02 / 5.17 ± 0.47 / 0.000745 ± 0.000139 / 0.81
24 / Diacyclops bicuspidatus / Panagrolaimus sp. / Nematode / No / 5.89E+01 / 3.00E-01 / 20 / 55.76 ± 19.19 / 0.000344 ± 0.0000527 / 0.71
25 / Mesocyclops edax / Brachionus calcyiflorus / Rotifer / No / 1.01E+02 / 3.35E+00 / 17 / 203.85 ± 124.32 / 0.87
26 / Mesocyclops edax / Asplanchna priodonta / Rotifer / No / 1.01E+02 / 1.13E+01 / 17 / 151.53 ± 188.61 / 0.0176 ± 0.00833 / 0.65
27 / Mesocyclops pehpeiensis / Brachionus rubens / Rotifer / No / 9.75E+01 / 5.23E-01 / 15 / 485.81 ± 120.83 / 0.0235 ± 0.0167 / 0.86
28 / Mesocyclops pehpeiensis / Brachionus rubens / Rotifer / No / 9.75E+01 / 5.23E-01 / 25 / 658.6 ± 89.84 / 0.97
29 / Mesocyclops pehpeiensis / Brachionus rubens / Rotifer / No / 9.75E+01 / 5.23E-01 / 35 / 323.18 ± 14.4 / 0.91
30 / Cyclops vicinus / Synchaeta spp. (S.oblonga and S.pectinata) / Rotifer / No / 9.41E+01 / 1.72E+00 / 15 / 88.13 ± 51.81 / 0.98
31 / Cyclops vicinus / Polyarthra spp. (P.vulgaris and P.dolichoptera) / Rotifer / No / 9.41E+01 / 4.50E-01 / 15 / 13.51 ± 4.18 / 0.0298 ± 0.0142 / 0.99
32 / Orthocyclops modestus / Urocentrum turbo / Ciliate / No / 2.87E+01 / 3.82E-01 / 18 / 42.87 ± 21 / 0.0501 ± 0.0172 / 0.51
33 / Orthocyclops modestus / Urocentrum turbo / Ciliate / No / 3.32E+01 / 3.82E-01 / 22 / 51.25 ± 4.68 / 0.159 ± 0.0512 / 0.79
34 / Orthocyclops modestus / Urocentrum turbo / Ciliate / No / 2.32E+01 / 3.82E-01 / 26 / 38.61 ± 5.46 / 0.268 ± 0.0728 / 0.54
35 / Mesocyclops thermocyclopoides / Anopheles stephensi - instar I / Insect / Yes / 6.58E+01 / 1.29E+01 / 25 / 371.31 ± 648.87 / 0.0234 ± 0.0127 / 0.73
36 / Mesocyclops thermocyclopoides / Culex quinquefasciatus - instar I / Insect / Yes / 6.58E+01 / 1.29E+01 / 25 / 362.37 ± 607.34 / 0.0593 ± 0.0216 / 0.67
37 / Mesocyclops thermocyclopoides / Anopheles stephensi - instar IV / Insect / Yes / 6.58E+01 / 1.14E+03 / 25 / 162.07 ± 180.1 / 0.00322 ± 0.0539 / 0.80
38 / Mesocyclops thermocyclopoides / Culex quinquefasciatus - instar IV / Insect / Yes / 6.58E+01 / 1.14E+03 / 25 / 63.84 ± 46.26 / 0.166 ± 0.143 / 0.90
39 / Acanthocyclops robustus / Synchaeta pectinata / Rotifer / No / 8.45E+01 / 1.72E+00 / 20 / 406.49 ± 579.76 / 0.0632 ± 0.47 / 0.97
40 / Acanthocyclops robustus / Daphnia hyalina / Cladocera / Yes / 8.45E+01 / 6.23E+01 / 20.75 / 175.47 ± 113.76 / 0.91
41 / Acanthocyclops robustus / Synchaeta kitina / Rotifer / No / 8.45E+01 / 4.00E-02 / 20.5 / 123.79 ± 359.91 / 0.96
42 / Acanthocyclops robustus / Brachionus calyciflorus / Rotifer / No / 8.45E+01 / 3.35E+00 / 21.75 / 61.44 ± 145.53 / 0.92
43 / Acanthocyclops robustus / Keratella cochlearis / Rotifer / No / 8.45E+01 / 2.50E-02 / 22.5 / 43.68 ± 333.51 / 0.74
44 / Acanthocyclops americanus / Acanthocyclops americanus nauplii / Copepod / Yes / 5.36E+01 / 25 / 47.48 ± 20.77 / 0.0868 ± 0.0333 / 0.96
45 / Acanthocyclops americanus / Brachionus havanaensis / Rotifer / No / 5.36E+01 / 2.00E+00 / 25 / 140.23 ± 147.65 / 0.0825 ± 0.0193 / 0.89
46 / Acanthocyclops americanus / Moina micrura / Cladocera / Yes / 5.36E+01 / 9.20E+00 / 25 / 60.25 ± 21.97 / 0.111 ± 0.029 / 0.97
47 / Megacyclops gigas / Copepd nauplii / Copepod / Yes / 3.75E+02 / 9.00E-01 / 20 / 17.87 ± 2.33 / 0.96
48 / Megacyclops gigas / Ceriodaphnia pulchella / Cladocera / Yes / 3.75E+02 / 1.83E+01 / 20 / 207.96 ± 188.34 / 0.92
49 / Megacyclops gigas / Cyclopoid copepodites / Copepod / Yes / 3.75E+02 / 6.50E+00 / 20 / 56.97 ± 24.72 / 0.96
50 / Megacyclops gigas / Daphnia galeata / Cladocera / Yes / 3.75E+02 / 3.36E+01 / 20 / 925.12 ± 1470.63 / 0.68

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