Evaluating food web interactions among microcrustaceans and insect in a tropical shallow lake using DNA-based protocol

References

• Agustí N, de Vicente MC, Gabarra R. 1999 Development of sequence amplified characterized region (SCAR) markers of Helicoverpa armigera: a new polymerase chain reaction–based technique for predator gut analysis. Mol Ecol. 8:1467–1474. doi: 10.1046/j.1365-294x.1999.00717.x.
   PubMed Web of Science ®Google Scholar
• Agustí N, de Vicente MC, Gabarra R. 2000. Developing SCAR markers to study predation on Trialeurodes vaporariorum. Insect Mol Biol. 9(3):263–268. doi: 10.1046/j.1365-2583.2000.00185.x.
   PubMed Web of Science ®Google Scholar
• Agustí N, Shayler SP, Harwood JD, Vaughan IP, Sunderland KD, Symondson WOC. 2003a. Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Mol Ecol. 12(12):3467–3475. doi: 10.1046/j.1365-294x.2003.02014.x.
   PubMed Web of Science ®Google Scholar
• Agustí N, Unruh TR, Welter SC. 2003b. Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers. Bull Entomol Res. 93(3):179–185. doi: 10.1079/BER2003236.
   PubMed Web of Science ®Google Scholar
• Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorol Z. 22(6):711–728. doi: 10.1127/0941-2948/2013/0507.
   Google Scholar
• Andersen NM. 1982. The semiaquatic bugs (Hemiptera: Gerromorpha) phylogeny, adaptations, biogeography and classification. Entomonograph. 3:1–455.
   Google Scholar
• Apte A, Daniel S. 2009. PCR primer design. Cold Spring Harb Protoc. 3:1–10.
   Google Scholar
• Arcifa MS. 2000. Feeding habits of Chaoboridae larvae in a tropical Brazilian reservoir. Braz J Biol. 60(4):591–597. doi: 10.1590/s0034-71082000000400008.
   PubMedGoogle Scholar
• Arcifa MS, Gomes EAT, Meschiatti AJ. 1992. Composition and fluctuations of the zooplankton of a tropical Brazilian reservoir. Arch hydrobiol. 123(4):479–495. doi: 10.1127/archiv-hydrobiol/123/1992/479.
   Google Scholar
• Arcifa MS, Meschiatti AJ, Gomes EAT. 1990. Thermal regime and stability of a tropical shallow reservoir: lake Monte Alegre. Brazil Rev Hydrobiol Trop. 23:271–281.
   Google Scholar
• Arcifa MS, Perticarrari A, Bunioto TC, Domingos AR and Minto WJ. 2016. Microcrustaceans and predators: diel migration in a tropical lake and comparison with shallow warm lakes. Limnetica. 35:281–296. doi: 10.23818/limn.35.23.
   Web of Science ®Google Scholar
• Arcifa MS, Santos Ferreira TC, Fileto C, Castilho-Noll MSM, Bunioto TC, Minto WJ. 2015. A long–term study on crustacean plankton of a shallow tropical lake: the role of invertebrate predation. J Limnol. 74:606–617. doi: 10.4081/jlimnol.2015.1132.
   Web of Science ®Google Scholar
• Arnér M, Koivisto S, Norberg J, Kautsky N. 1998. Trophic interactions in rockpool food webs regulation of zooplankton and phytoplankton by Notonecta and Daphnia. Freshwater Biol. 39(1):79–90. doi: 10.1046/j.1365-2427.1998.00262.x.
   Web of Science ®Google Scholar
• Asahida T, Yamashita Y, Kobayashi T. 1997. Identification of consumed stone flounder, Kareius bicoloratus (Basilewsky), from the stomach contents of sand shrimp, Crangon affinis (De Haan) using mitochondrial DNA analysis. J Exp Mar Bio Ecol. 217(2):153–163. doi: 10.1016/S0022-0981(97)00039-7.
   Web of Science ®Google Scholar
• Balseiro EG. 1992. The role of pelagic water mites in the control of cladoceran population in a temperate lake of the southern Andes. J Plankton Res. 14(9):1267–1277. doi: 10.1093/plankt/14.9.1267.
   Web of Science ®Google Scholar
• Blankenship LE, Yayanos AA. 2005. Universal primers and PCR of gut contents to study marine invertebrate diets. Mol Ecol. 14(3):891–899. doi: 10.1111/j.1365-294X.2005.02448.x.
   PubMed Web of Science ®Google Scholar
• Blaustein L. 1998. Influence of the predatory backswimmer, Notonecta maculata, on invertebrate community structure. Ecol Entom. 23:246–252.
   Web of Science ®Google Scholar
• Bulgarini G, Piemontese L, Guidetti R, Cesari M, di Bella E, Maistrello L. 2022. Identification of predatory arthropods of the invasive Halyomorpha halys through molecular gut content analysis. Agric For Entomol. 24(2):219–228. doi: 10.1111/afe.12485.
   Web of Science ®Google Scholar
• Carreon-Martinez L, Johnson TB, Ludsin SA, Heath DD. 2011. Utilization of stomach content DNA to determine diet diversity in piscivorous fishes. J Fish Biol. 78(4):1170–1182. doi: 10.1111/j.1095-8649.2011.02925.x.
   PubMed Web of Science ®Google Scholar
• Cassano CR, Castilho-Noll MSM, Arcifa MS. 2002. Water mite predation on zooplankton of a tropical lake. Braz J Biol. 62(4A):565–571. doi: 10.1590/s1519-69842002000400002.
   PubMedGoogle Scholar
• Castilho-Noll MSM, Arcifa MS. 2007a. Chaoborus diet in a tropical lake and predation of microcrustaceans in laboratory experiments. Acta Limnol Bras. 19:163–174.
   Google Scholar
• Castilho-Noll MSM, Arcifa MS. 2007b. Mesocosm experiment on the impact of invertebrate predation on zooplankton of a tropical lake. Aquat Ecol. 41(4):587–598. doi: 10.1007/s10452-007-9112-4.
   Web of Science ®Google Scholar
• Caterino MS, Cho S, Sperling FA. 2000. The current state of insect molecular systematics: a thriving Tower of Babel. Annu Rev Entomol. 45(1):1–54. doi: 10.1146/annurev.ento.45.1.1.
   PubMedGoogle Scholar
• Clare EL, Fraser EE, Braid HE, Fenton MB, Hebert PDN. 2009. Species on the menu of a generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect arthropod prey. Mol Ecol. 18(11):2532–2542. doi: 10.1111/j.1365-294X.2009.04184.x.
   PubMed Web of Science ®Google Scholar
• Cummins KW. 1973. Trophic relations of aquatic insects. Annu Rev Entomol. 18(1):183–206. doi: 10.1146/annurev.en.18.010173.001151.
   Google Scholar
• Deagle BE, Gales NJ, Evans K, Jarman SN, Robinson S, Trebilco R, Hindell MA. 2007. Studying seabird diet through genetic analysis of faeces: a case study on macaroni penguins (Eudyptes chrysolophus). PLoS One. 2(9):e831. doi: 10.1371/journal.pone.0000831.
   PubMed Web of Science ®Google Scholar
• Deagle BE, Kirkwood R, Jarman SN. 2009. Analysis of Australian fur seal diet by pyrosequencing prey DNA in feces. Mol Ecol. 18(9):2022–2038. doi: 10.1111/j.1365-294X.2009.04158.x.
   PubMed Web of Science ®Google Scholar
• Deagle BE, Tollit DJ. 2007. Quantitative analysis of prey DNA in pinniped faeces: potential to estimate diet composition? Conserv Genet. 8(3):743–747. doi: 10.1007/s10592-006-9197-7.
   Web of Science ®Google Scholar
• Deagle BE, Tollit DJ, Jarman SN, Hindell MA, Trites AW, Gales NJ. 2005. Molecular scatology as a tool to study diet: analysis of prey DNA in scats from captive Steller sea lions. Mol Ecol. 14(6):1831–1842. doi: 10.1111/j.1365-294X.2005.02531.x.
   PubMed Web of Science ®Google Scholar
• Dieffenbach CW, Lowe TM, Dveksler GS. 1993. General concepts for PCR primer design. PCR Methods Appl. 3(3):S30–S37. doi: 10.1101/gr.3.3.s30.
   PubMedGoogle Scholar
• Domingos AR, Arcifa MS. 2017a. Spatial and temporal distribution of gerrid (Heteroptera) and predation on microcrustaceans from a tropical shallow lake. Braz J Biol. 77(2):289–298. doi: 10.1590/1519-6984.12715.
   PubMed Web of Science ®Google Scholar
• Domingos AR, Arcifa MS. 2017b. Distribution and fluctuations of backswimmers (Notonectidae) in a tropical shallow lake and predation on microcrustaceans. Braz J Biol. 1:117. doi: 10.1590/1519-6984.10815.
   PubMed Web of Science ®Google Scholar
• Estoup A, Largiader CR, Perrot E, Chourrout D. 1996. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Mar Biol Biotechnol. 5:295–298.
   Google Scholar
• Folmer OO, Black MM, Hoeh WW, Lutz RR, Vrijenhoek RR. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 3:294–299.
   PubMedGoogle Scholar
• Gamboa M, Kimbirauskas RK, Merritt RW, Monaghan MT. 2012. A Molecular approach to identifying the natural prey of the African creeping water bug Naucoris, a potential reservoir of Mycobacterium ulcerans. J Insect Sci. 12(2):2–10. doi: 10.1673/031.012.0201.
   PubMedGoogle Scholar
• Garrison JA, Motwani NH, Broman E, Nascimento FJ. 2022. Molecular diet analysis enables detection of diatom and cyanobacteria DNA in the gut of Macoma balthica. PLoS One. 17(11):e0278070. doi: 10.1371/journal.pone.0278070.
   PubMed Web of Science ®Google Scholar
• Gliwicz ZM, Pijanowska J. 1989. The role of predation in zooplankton succession. In: Sommer U, editor. Plankton Ecology: succession in plankton communities. Heidelberg (DE–BE): Springer-Verlag; p. 253–296.
   Google Scholar
• Greenstone MH, Shufran KA. 2003. Spider predation: species–specific identification of gut contents by polymerase chain reaction. J Arachnol. 31(1):131–134. doi: 10.1636/0161-8202(2003)031[0131:SPSIOG.2.0.CO;2]
   Web of Science ®Google Scholar
• Hajibabaei M, Smith MA, Janzen DH, Rodriguez JJ, Whitfield JB, Hebert PDN. 2006. A minimalist barcode can identify a specimen whose DNA is degraded. Mol Ecol Notes. 6(4):959–964. doi: 10.1111/j.1471-8286.2006.01470.x.
   Web of Science ®Google Scholar
• Hall TA. 2005. BioEdit 7.0.5 Department of Microbiology, North Carolina State University, Raleigh, NC, USA https://bioedit.software.informer.com/7.2/.
   Google Scholar
• Harper GL, King RA, Dodd CS, Harwood JD, Glen DM, Bruford MW, Symondson WOC. 2005. Rapid screening of invertebrate predators for multiple prey DNA targets. Mol Ecol. 14(3):819–827. doi: 10.1111/j.1365-294X.2005.02442.x.
   PubMed Web of Science ®Google Scholar
• Hebert PDN, Cywinska A, Ball SL, de Waard JR. 2003a. Biological identifications through DNA barcodes. Proc Biol Sci. 270(1512):313–321. doi: 10.1098/rspb.2002.2218.
   PubMed Web of Science ®Google Scholar
• Hebert PDN, Ratnasingham S, de Waard JR. 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc B Biol Sci. 270:S96–S99.
   PubMed Web of Science ®Google Scholar
• Hoogendoorn M, Heimpel GE. 2001. PCR-based gut content analysis of insect predators: using ribosomal ITS–1 fragments from prey to estimate predation frequency. Mol Ecol. 10(8):2059–2067. doi: 10.1046/j.1365-294x.2001.01316.x.
   PubMed Web of Science ®Google Scholar
• Hoy MA. 2003. Insect molecular genetics: an introduction to principals and applications. San Diego (CA): Academic Press; p. 544.
   Google Scholar
• Jara FG, Perotti MG, Diéguez MC. 2012. Distribution of backswimmers in shallow ponds of Patagonia and their predatory role on a common tadpole–copepod assemblage. New Zeal J Mar Fresh. 46(4):459–473. doi: 10.1080/00288330.2012.707130.
   Web of Science ®Google Scholar
• Jarman SN. 2004. Amplicon: software for designing PCR primers on aligned DNA sequences. Bioinformatics. 20(10):1644–1645. doi: 10.1093/bioinformatics/bth121.
   PubMed Web of Science ®Google Scholar
• Jarman SN, Deagle BE, Gales NJ. 2004. Group-specific polymerase chain reaction for DNA–based analysis of species diversity and identity in dietary samples. Mol Ecol. 13(5):1313–1322. doi: 10.1111/j.1365-294X.2004.02109.x.
   PubMed Web of Science ®Google Scholar
• Jarman SN, Gales NJ, Tierney M, Gill PC, Elliott NG. 2002. A DNA-based method for identification of krill species and its application to analysing the diet of marine vertebrate predators. Mol Ecol. 11(12):2679–2690. doi: 10.1046/j.1365-294x.2002.01641.x.
   PubMed Web of Science ®Google Scholar
• Jarman SN, Redd KS, Gales NJ. 2006. Group-specific primers for amplifying DNA sequences that identify Amphipoda, Cephalopoda, Echinodermata, Gastropoda, Isopoda, Ostracoda and Thoracica. Mol Ecol Notes. 6(1):268–271. doi: 10.1111/j.1471-8286.2005.01172.x.
   Google Scholar
• King RA, Read DS, Traugott M, Symondson WOC. 2008. Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol. 17(4):947–963. doi: 10.1111/j.1365-294X.2007.03613.x.
   PubMed Web of Science ®Google Scholar
• King RA, Vaughan IP, Bell JR, Bohan DA, Symondson WOC. 2010. Prey choice by carabid beetles feeding on an earthworm community analysed using species– and lineage–specific PCR primers. Mol Ecol. 19(8):1721–1732. doi: 10.1111/j.1365-294X.2010.04602.x.
   PubMed Web of Science ®Google Scholar
• Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA. 86(16):6196–6200. doi: 10.1073/pnas.86.16.6196.
   PubMed Web of Science ®Google Scholar
• Korbie DJ, Mattick JS. 2008. Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat Protoc. 3(9):1452–1456. doi: 10.1038/nprot.2008.133.
   PubMed Web of Science ®Google Scholar
• Lundgren JG, Ellsbury ME, Prischmann DA. 2009. Analysis of the predator community of a subterranean herbivorous insect based on polymerase chain reaction. Ecol Appl. 19(8):2157–2166. doi: 10.1890/08-1882.1.
   PubMed Web of Science ®Google Scholar
• Meusnier I, Singer GC, Landry JF, Hickey DA, Hebert PDN, Hajibabaei M. 2008. A universal DNA mini-barcode for biodiversity analysis. BMC Genomics. 9(1):214. doi: 10.1186/1471-2164-9-214.
   PubMedGoogle Scholar
• Minto WJ, Arcifa MS, Perticarrari A. 2010. Experiments on the influence of Chaoborus brasiliensis Theobald, 1901 (Diptera: Chaoboridae) on the diel vertical migration of microcrustaceans from Lake Monte Alegre. Braz J Biol. 70(1):25–35. doi: 10.1590/s1519-69842010000100006.
   PubMed Web of Science ®Google Scholar
• Moore MV, Gilbert JJ. 1987. Age-specific Chaoborus predation on rotifer prey. Freshwater Biol. 17(2):223–236. doi: 10.1111/j.1365-2427.1987.tb01044.x.
   Web of Science ®Google Scholar
• Mumm H. 1997. Effects of competitors and Chaoborus predation on the cladocerans of a eutrophic lake: an enclosure study. Hydrobiologia. 360(1/3):253–264. doi: 10.1023/A:1003177622210.
   Google Scholar
• Nejstgaard JC, Frischer ME, Simonelli P, Troedsson C, Brakel M, Adiyaman F, Sazhin AF, Artigas FL. 2008. Quantitative PCR to estimate copepod feeding. Mar Biol. 153(4):565–577. doi: 10.1007/s00227-007-0830-x.
   Web of Science ®Google Scholar
• Palero F, Hall S, Clark PF, Johnston D, Mackenzie-Dodds J, Thatje S. 2010. DNA extraction from formalin-fixed tissue: new light from the deep sea. Sci Mar. 74(3):465–470. doi: 10.3989/scimar.2010.74n3465.
   Web of Science ®Google Scholar
• Palumbi SR. 1996. Nucleic acids II: the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK, editors. Molecular systematics. 2nd ed. Sinauer, Sunderland (MA); p. 655.
   Google Scholar
• Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G. 1991. The simple fool’s guide to PCR, Version 2.0. HI: University of Hawaii; p. 45.
   Google Scholar
• Peckarsky BL. 1982. Aquatic insect predator–prey relations. Bioscience. 32(4):261–266. doi: 10.2307/1308532.
   Web of Science ®Google Scholar
• Piñol J, San Andrés V, Clare EL, Mir G, Symondson WOC. 2014. A pragmatic approach to the analysis of diets of generalist predators: the use of next–generation sequencing with no blocking probes. Mol Ecol Resour. 14(1):18–26. doi: 10.1111/1755-0998.12156.
   PubMed Web of Science ®Google Scholar
• Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P. 2012. Who is eating what: diet assessment using next generation sequencing. Mol Ecol. 21(8):1931–1950. doi: 10.1111/j.1365-294X.2011.05403.x.
   PubMed Web of Science ®Google Scholar
• Ratnasingham S, Hebert PDN. 2007. Bold: the barcode of life data system (http://www.barcodinglife.org). Mol Ecol Notes. 7(3):355–364. doi: 10.1111/j.1471-8286.2007.01678.x.
   PubMed Web of Science ®Google Scholar
• Sheppard SK, Harwood JD. 2005. Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Funct Ecol. 19(5):751–762. doi: 10.1111/j.1365-2435.2005.01041.x.
   Web of Science ®Google Scholar
• Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am. 87(6):651–701. doi: 10.1093/aesa/87.6.651.
   Web of Science ®Google Scholar
• Simonelli P, Troedsson C, Nejstgaard JC, Zech K, Larsen JB, Frischer ME. 2009. Evaluation of DNA extraction and handling procedures for PCR-based copepod feeding studies. J Plankton Res. 31(12):1465–1474. doi: 10.1093/plankt/fbp087.
   Web of Science ®Google Scholar
• Singh VK, Kumar A. 2001. PCR primer design. Mol Biol Today. 2:27–32.
   Google Scholar
• Soininen EM, Valentini A, Coissac E, Miquel C, Gielly L, Brochmann C, Brysting AK, Sønstebø JH, Ims RA, Yoccoz NG, et al. 2009. Analysing diet of small herbivores: the efficiency of DNA barcoding coupled with high-throughput pyrosequencing for deciphering the composition of complex plant mixtures. Front Zool. 6(1):16. doi: 10.1186/1742-9994-6-16.
   PubMedGoogle Scholar
• Spence JR, Anderson NM. 1994. Biology of water striders: interactions between systematics and ecology. Annu Rev Entomol. 39(1):101–128. doi: 10.1146/annurev.en.39.010194.000533.
   Google Scholar
• Streams FA. 1987. Foraging behavior in a notonectid assemblage. Am Midl Nat. 117(2):353–361. doi: 10.2307/2425977.
   Web of Science ®Google Scholar
• Symondson WOC. 2002. Molecular identification of prey in predator diets. Mol Ecol. 11(4):627–641. doi: 10.1046/j.1365-294x.2002.01471.x.
   PubMed Web of Science ®Google Scholar
• Taguchi T, Miura Y, Krueger D, Sugiura S. 2014. Utilizing stomach content and faecal DNA analysis techniques to assess the feeding behaviour of largemouth bass Micropterus salmoides and bluegill Lepomis macrochirus. J Fish Biol. 84(5):1271–1288. doi: 10.1111/jfb.12341.
   PubMed Web of Science ®Google Scholar
• Tiede J, Wemheuer B, Traugott M, Daniel R, Tscharntke T, Ebeling A, Scherber C. 2016. Trophic and non-trophic interactions in a biodiversity experiment assessed by next-generation sequencing. PLoS One. 11(2):e0148781. doi: 10.1371/journal.pone.0148781.
   PubMed Web of Science ®Google Scholar
• Töbe K, Meyer B, Fuentes V. 2010. Detection of zooplankton items in the stomach and gut content of larval krill, Euphausia superba, using a molecular approach. Polar Biol. 33(3):407–414. doi: 10.1007/s00300-009-0714-2.
   Web of Science ®Google Scholar
• Vestheim H, Edvardsen B, Kaartvedt S. 2005. Assessing feeding of a carnivorous copepod using species-specific PCR. Mar Biol. 147(2):381–385. doi: 10.1007/s00227-005-1590-0.
   Web of Science ®Google Scholar
• Vestheim H, Jarman SN. 2008. Blocking primers to enhance PCR amplification of rare sequences in mixed samples – a case study on prey DNA in Antarctic krill stomachs. Front Zool. 5(1):12. doi: 10.1186/1742-9994-5-12.
   PubMedGoogle Scholar
• Wilson DS. 1975. The adequacy of body size as a niche difference. Am Nat. 109(970):769–784. doi: 10.1086/283042.
   Web of Science ®Google Scholar
• Xiao D, Xu Q, Chen X, Du X, Desneux N, Thomine E, Hui-Jie D, Harwood J, Wang S. 2021. Development of a molecular gut-content identification system to identify aphids preyed upon by the natural enemy Coccinella septempunctata. Entomologia. 41(6):591–599. doi: 10.1127/entomologia/2021/1032.
   Google Scholar
• Young JD, Riessen HP. 2005. The interaction of Chaoborus size and vertical distribution determines predation effects on Daphnia. Fresh Biol. 50(6):993–1006. doi: 10.1111/j.1365-2427.2005.01381.x.
   Web of Science ®Google Scholar
• Zaidi RH, Jaal Z, Hawkes NJ, Hemingway J, Symondson WOC. 1999. Can multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators? Mol Ecol. 8(12):2081–2087. doi: 10.1046/j.1365-294x.1999.00823.x.
   PubMed Web of Science ®Google Scholar
• Zarzoso-Lacoste D, Corse E, Vidal E. 2013. Improving PCR detection of prey in molecular diet studies: importance of group-specific primer set selection and extraction protocol performances. Mol Ecol Resour. 13(1):117–127. doi: 10.1111/1755-0998.12029.
   PubMed Web of Science ®Google Scholar
• Zeale MRK, Butlin RK, Barker GLA, Lees DC, Jones G. 2011. Taxon-specific PCR for DNA barcoding arthropod prey in bat feces. Mol Ecol Resour. 11(2):236–244. doi: 10.1111/j.1755-0998.2010.02920.x.
   PubMed Web of Science ®Google Scholar