Different feeding preferences for macronutrients across seasons and sites indicate temporal and spatial nutrient limitation in the black bog ant
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
ATCZ214
Interreg
PubMed
38635052
DOI
10.1007/s00442-024-05545-8
PII: 10.1007/s00442-024-05545-8
Knihovny.cz E-zdroje
- Klíčová slova
- Field experiment, Food resources, Formicidae, Nutrition, Temporal variance,
- MeSH
- Formicidae * fyziologie MeSH
- mokřady MeSH
- preference v jídle MeSH
- roční období * MeSH
- stravovací zvyklosti MeSH
- živiny * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
How the resource use by consumers vary in different environments and time scales is one of the fundamental ecological questions. Replicated field studies are rare, however; so the extent to which nutrient use varies and why is uncertain. We studied an endangered tyrphobiotic species, the black bog ant (Formica picea), and its feeding preferences in temperate peatlands. We conducted a baiting experiment at three different sites with high nest densities, repeated over three years and three periods of growing season. Preferences for three main macronutrients (carbohydrates, proteins and lipids) were assessed. We hypothesised that if nutrient limitation plays a role, ants will have an increased need for proteins and lipids in early seasons when brood is raised, while carbohydrates use will increase in late seasons. We also expected that site identity would influence nutrient preferences, but not year. Our results supported the nutrient limitation hypothesis for proteins that were consumed more in the early season. In contrast, preference for carbohydrates was rather high and did not increase consistently through season. Although the occupancy of lipid baits was low overall, it increased at colder temperatures, in contrast to carbohydrate and protein baits. Nutrient preferences varied more among sites than years, with the lowest nutrient use observed in a diverse fen-meadow, consistent with the nutrient limitation hypothesis. Year affected ant abundance, but not bait occupancy. Our results suggest that black bog ants flexibly adapt their diet to environmental conditions and that an interplay between nutrient limitation and climate determines their feeding behaviour.
Institute of Botany of the Czech Academy of Sciences Dukelská 135 379 01 Třeboň Czech Republic
Muzeum Vysočiny Jihlava Masarykovo náměstí 55 586 01 Jihlava Czech Republic
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Abbott KL, Green PT, O’Dowd DJ (2014) Seasonal shifts in macronutrient preferences in supercolonies of the invasive yellow crazy ant Anoplolepis gracilipes (Smith, 1857) (Hymenoptera: Formicidae) on Christmas Island, Indian Ocean. Austral Entomol 53:337–346. https://doi.org/10.1111/aen.12081 DOI
Agren GI, Wetterstedt JAM, Billberger MFK (2012) Nutrient limitation on terrestrial plant growth––modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960. https://doi.org/10.1111/j.1469-8137.2012.04116.x PubMed DOI
Batzer DP, Wissinger SA (1996) Ecology of insect communities in nontidal wetlands. Annu Rev Entomol 41:75–100. https://doi.org/10.1146/annurev.en.41.010196.000451 PubMed DOI
Bezděčková K, Bezděčka P (2011) Endangered non-forest Formica. Formica picea, Formica exsecta, Formica foreli and Formica pressilabris [In Czech and English]. Muzeum Vysočiny Jihlava, Czech Republic.
Bezděčková K, Bezděčka P, Fibich P, Klimeš P (2024) Data and code: Different feeding preferences for macronutrients across seasons and sites indicate temporal and spatial nutrient limitation in the black bog ant (1.0). Zenodo. https://doi.org/10.5281/zenodo.10955836
Blackman RL, Eastop VF (2006) Aphids on the world’s herbaceous plants and shrubs. Wiley, Chichester
Boggs CL (2009) Understanding insect life histories and senescence through a resource allocation lens. Funct Ecol 23:27–37. https://doi.org/10.1111/j.1365-2435.2009.01527.x DOI
Bönner W (1915) Die Überwintering von Formica fusca picea und andere biologische Beobachtungen. Biologisches Centralblatt 35:65–77
Bridgham SD, Pastor J, Janssens JA, Chapin C, Malterer TJ (1996) Multiple limiting gradients in peatlands: A call for a new paradigm. Wetlands 16:45–65. https://doi.org/10.1007/bf03160645 DOI
Cardoso P, Silva I, De Oliveira NG, Serrano ARM (2007) Seasonality of spiders (Araneae) in Mediterranean ecosystems and its implications in the optimum sampling period. Ecol Entomol 32:516–526. https://doi.org/10.1111/j.1365-2311.2007.00894.x DOI
Carscallen G (2019) Arthropod Diversity in Contrasting Ontario Peatlands. Electronic Thesis and Dissertation Repository. 6703. The University of Western Ontario. https://ir.lib.uwo.ca/etd/6703/
Čech L, Šumpich J, Zabloudil V (2002) Jihlavsko. In: Mackovčin P, Sedláček M (eds) Chráněná území ČR, svazek VII. Praha, AOPK ČR a Ekocentrum Brno, pp 237–429
Cerda X, Retana J, Cros S (1998) Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance. Funct Ecol 12:45–55. https://doi.org/10.1046/j.1365-2435.1998.00160.x DOI
Chytrý M et al (2021) Pladias database of the Czech flora and vegetation. Preslia 93(1):1–87 DOI
Cook SC, Eubanks MD, Gold RE, Behmer ST (2011) Seasonality directs contrasting food collection behavior and nutrient regulation strategies in ants. PLoS ONE. https://doi.org/10.1371/journal.pone.0025407 PubMed DOI PMC
Csata E, Dussutour A (2019) Nutrient regulation in ants (Hymenoptera: Formicidae): a review. Myrmecol News 29:111–124
Cumming GS, Ndlovu M, Mutumi GL, Hockey PAR (2013) Responses of an African wading bird community to resource pulses are related to foraging guild and food-web position. Freshw Biol 58:79–87. https://doi.org/10.1111/fwb.12040 DOI
Czaczkes TJ, Ratnieks FLW (2013) Cooperative transport in ants (Hymenoptera: Formicidae) and elsewhere. Myrmecol News 18:1–11
Czechowski W, Radchenko A, Czechowska W, Vepsäläinen K (2012) The ants of Poland with reference to the myrmecofauna of Europe. Natura optima dux Foundation, Poland
Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linnean Soc 61:153–181. https://doi.org/10.1006/bijl.1996.0128 DOI
De Cuyper A et al (2023) Nutrient intake and its possible drivers in free-ranging European brown bears (Ursus arctos arctos). Ecol Evol 13:15. https://doi.org/10.1002/ece3.10156 DOI
Dlussky GM (2001) Season dynamic of brood development of Formica candida colonies from isolated bog population. In: Ants and forest protection: materials of the 11th All-Russian Myrmecological Symposium, Perm, pp 69–71 [Conference proceedings in Russian with abstract in English]. Permsky gosudarstvennyj universitet, Perm.
Domisch T et al (2009) Foraging activity and dietary spectrum of wood ants and their role in nutrient fluxes in boreal forests. Ecol Entomol 34:369–377. https://doi.org/10.1111/j.1365-2311.2009.01086.x DOI
Dunn PO, Winkler DW, Whittingham LA, Hannon SJ, Robertson RJ (2011) A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92:450–461. https://doi.org/10.1890/10-0478.1 PubMed DOI
Feldhaar H (2014) Ant nutritional ecology: linking the nutritional niche plasticity on individual and colony-level to community ecology. Curr Opin Insect Sci 5:25–30. https://doi.org/10.1016/j.cois.2014.09.007 PubMed DOI
Fellers JH (1989) Daily and seasonal activity in woodland ants. Oecologia 78:69–76. https://doi.org/10.1007/BF00377199 PubMed DOI
Fernandez-Tizon M, Emmenegger T, Perner J, Hahn S (2020) Arthropod biomass increase in spring correlates with NDVI in grassland habitat. Sci Nat. https://doi.org/10.1007/s00114-020-01698-7 DOI
Fiedler K, Kuhlmann F, Schlick-Steiner BC, Steiner FM, Gebauer G (2007) Stable N-isotope signatures of central European ants––assessing positions in a trophic gradient. Insectes Soc 54:393–402. https://doi.org/10.1007/s00040-007-0959-0 DOI
Fisher JB, Badgley G, Blyth E (2012) Global nutrient limitation in terrestrial vegetation. Glob Biogeochem Cycle 26:9. https://doi.org/10.1029/2011gb004252 DOI
Guariento E, Martini J, Fiedler K (2018) Bait visitation by Formica lemani (Hymenoptera: Fomicidae) indicates shortage of carbohydrates in alpine grasslands. Eur J Entomol 115:217–222. https://doi.org/10.14411/eje.2018.020 DOI
Guariento E, Wanek W, Fiedler K (2021) Consistent shift in nutritional ecology of ants reveals trophic flexibility across alpine tree-line ecotones. Ecol Entomol 46:1082–1092. https://doi.org/10.1111/een.13052 DOI
Haddad NM, Tilman D, Haarstad J, Ritchie M, Knops JMH (2001) Contrasting effects of plant richness and composition on insect communities: a field experiment. Am Nat 158:17–35. https://doi.org/10.1086/320866 PubMed DOI
Hahn DA, Wheeler DE (2002) Seasonal foraging activity and bait preferences of ants on Barro Colorado Island, Panama. Biotropica 34:348–356 DOI
Hakala SM, Meurville MP, Stumpe M, LeBoeuf AC (2021) Biomarkers in a socially exchanged/fluid reflect colony maturity, behavior, and distributed metabolism. Elife. https://doi.org/10.7554/eLife.74005 PubMed DOI PMC
Hallmann CA et al (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE. https://doi.org/10.1371/journal.pone.0185809 PubMed DOI PMC
Heinze J, Foitzik S, Fischer B, Wanke T, Kipyatkov VE (2003) The significance of latitudinal variation in body size in a holarctic ant, Leptothorax acervorum. Ecography 26:349–355. https://doi.org/10.1034/j.1600-0587.2003.03478.x DOI
Hopkins GW (1996) A local hoverfly and a rare aphid tended by an endangered ant on cottongrass. In: Morgan IK (ed) Newsletter No 33. Dyfed invertebrate group, Cairns, Australia
Horstmann K (1972) Investigations on food consumption of red wood ants (Formica polyctena Foerster) in oak forest: effect of season and supply of food. Oecologia 8(4):371–390. [In German with English abstract] https://doi.org/10.1007/bf00367539 PubMed DOI
Hoshikawa T (1981) Some colony factors influencing the hunting activity of Polistes chinensis antennalis Perez (Hymenoptera, Vespidae). Appl Entomol Zool 16:395–405. https://doi.org/10.1303/aez.16.395 DOI
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425 PubMed DOI
Hou R et al (2021) The geometry of resource constraint: an empirical study of the golden snub-nosed monkey. J Anim Ecol 90:751–765. https://doi.org/10.1111/1365-2656.13408 PubMed DOI
Iakovlev IK, Novgorodova TA, Tiunov AV, Reznikova ZI (2017) Trophic position and seasonal changes in the diet of the red wood ant Formica aquilonia as indicated by stable isotope analysis. Ecol Entomol 42:263–272. https://doi.org/10.1111/een.12384 DOI
Jassey VEJ, Shimano S, Dupuy C, Toussaint ML, Gilbert D (2012) Characterizing the feeding habits of the testate Amoebae Hyalosphenia papilio and Nebela tincta along a narrow “Fen-Bog” gradient using digestive vacuole content and C-13 and N-15 isotopic analyses. Protist 163:451–464. https://doi.org/10.1016/j.protis.2011.07.006 PubMed DOI
Jensen K et al (2012) Optimal foraging for specific nutrients in predatory beetles. Proc R Soc Lond Ser B-Biol Sci 279:2212–2218. https://doi.org/10.1098/rspb.2011.2410 DOI
Judd TM (2005) The effects of water, season, and colony composition on foraging preferences of Pheidole ceres (Hymenoptera : Formicidae). J Insect Behav 18:781–803. https://doi.org/10.1007/s10905-005-8740-6 DOI
Kapyla M (1978) Amount and type of nectar sugar in some wild flowers in Finland. Ann Bot Fenn 15:85–88
Kaspari M (2020) The seventh macronutrient: how sodium shortfall ramifies through populations, food webs and ecosystems. Ecol Lett 23:1153–1168. https://doi.org/10.1111/ele.13517 PubMed DOI
Kaspari M, Yanoviak SP (2001) Bait use in tropical litter and canopy ants - evidence of differences in nutrient limitation. Biotropica 33:207–211. https://doi.org/10.1111/j.1744-7429.2001.tb00172.x DOI
Kaspari M, Donoso D, Lucas JA, Zumbusch T, Kay AD (2012) Using nutritional ecology to predict community structure: a field test in Neotropical ants. Ecosphere 3:15. https://doi.org/10.1890/es12-00136.1 DOI
Kavle RR, Nolan PJ, Carne A, Agyei D, Morton JD, Bekhit AEA (2023) Earth Worming An Evaluation of Earthworm (Eisenia andrei) as an Alternative Food Source. Foods. https://doi.org/10.3390/foods12101948 PubMed DOI PMC
Konecna M, Moos M, Zahradnickova H, Simek P, Leps J (2018) Tasty rewards for ants: differences in elaiosome and seed metabolite profiles are consistent across species and reflect taxonomic relatedness. Oecologia 188:753–764. https://doi.org/10.1007/s00442-018-4254-8 PubMed DOI
Krab EJ, Berg MP, Aerts R, van Logtestijn RSP, Cornelissen JHC (2013) Vascular plant litter input in subarctic peat bogs changes collembola diets and decomposition patterns. Soil Biol Biochem 63:106–115. https://doi.org/10.1016/j.soilbio.2013.03.032 DOI
Lach L, Parr LC, Abbott KL (2010) Ant Ecology. Oxford University Press Inc., New York
Lasmar CJ, Bishop TR, Parr CL, Queiroz ACM, Schmidt FA, Ribas CR (2021) Geographical variation in ant foraging activity and resource use is driven by climate and net primary productivity. J Biogeogr 48:1448–1459. https://doi.org/10.1111/jbi.14089 DOI
Lasmar CJ et al (2023) Testing the context dependence of ant nutrient preference across habitat strata and trophic levels in Neotropical biomes. Ecology 104:e3975. https://doi.org/10.1002/ecy.3975 PubMed DOI
Law SJ, Parr C (2020) Numerically dominant species drive patterns in resource use along a vertical gradient in tropical ant assemblages. Biotropica 52:101–112. https://doi.org/10.1111/btp.12743 DOI
Lee KP et al (2008) Lifespan and reproduction in Drosophila: New insights from nutritional geometry. Proc Natl Acad Sci U S A 105:2498–2503. https://doi.org/10.1073/pnas.0710787105 PubMed DOI PMC
Lenoir L (2002) Can wood ants distinguish between good and bad food patches on the forest floor? Eur J Soil Biol 38:97–102. https://doi.org/10.1016/s1164-5563(01)01113-x DOI
Li XP et al (2019) Effects of two natural diets on the response of the predator Arma chinensis (Hemiptera: Pentatomidae: Asopinae) to cold storage. Appl Ecol Environ Res 17:15329–15347. https://doi.org/10.15666/aeer/1706_1532915347 DOI
Mabelis AA, Chardon JP (2005) Survival of the black bog ant (Formica trankaucasica Nasanov) in relation to the fragmentation of its habitat. J Insect Conser 9(2):95–108. https://doi.org/10.1007/s10841-004-5987-8 DOI
Machovsky-Capuska GE, Senior AM, Simpson SJ, Raubenheimer D (2016) The multidimensional nutritional niche. Trends Ecol Evol 31:355–365. https://doi.org/10.1016/j.tree.2016.02.009 PubMed DOI
Mailleux AC, Deneubourg JL, Detrain C (2000) How do ants assess food volume? Anim Behav 59:1061–1069. https://doi.org/10.1006/anbe.2000.1396 PubMed DOI
Marsh KJ, Blyton MDJ, Foley WJ, Moore BD (2021) Fundamental dietary specialisation explains differential use of resources within a koala population. Oecologia 196:795–803. https://doi.org/10.1007/s00442-021-04962-3 PubMed DOI
Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113. https://doi.org/10.1126/science.1105493 PubMed DOI
Mieczan T, Adamczuk M, Pawlik-Skowronska B, Toporowska M (2015) Eutrophication of peatbogs: consequences of P and N enrichment for microbial and metazoan communities in mesocosm experiments. Aquat Microb Ecol 74:121–141. https://doi.org/10.3354/ame01727 DOI
Minayeva T et al (2008) Peatlands and biodiversity. Assessment on Peatlands, Biodiversity and Climate Change. Global Environment Centre, Kuala Lumpur & Wetlands International, pp 60–98
Mony R, Dejean A, Bilong CFB, Kenne M, Rouland-Lefèvre C (2013) Melissotarsus ants are likely able to digest plant polysaccharides. C R Biol 336:500–504. https://doi.org/10.1016/j.crvi.2013.08.003 PubMed DOI
Moses J et al (2023) Nutrient use by tropical ant communities varies among three extensive elevational gradients: a cross-continental comparison. Glob Ecol Biogeogr 32(12):2212–2229. https://doi.org/10.1111/geb.13757 DOI
Nielsen SMB, Bilde T, Toft S (2022) Macronutrient niches and field limitation in a woodland assemblage of harvestmen. J Anim Ecol 91:593–603. https://doi.org/10.1111/1365-2656.13649 PubMed DOI
Novak H (1994) The influence of ant attendance on larval parasitism in hawthorn psyllids (Homoptera, Psyllidae). Oecologia 99:72–78. https://doi.org/10.1007/bf00317085 PubMed DOI
O’Hara RB, Kotze DJ (2010) Do not log-transform count data. Methods Ecol Evol 1:118–122. https://doi.org/10.1111/j.2041-210X.2010.00021.x DOI
R Core Team (2022) R: A Language and Environment for Statistical Computing. Ver. 4.2.2. R Foundation for Statistical Computing, Vienna, Austria
Remonti L, Balestrieri A, Prigioni C (2011) Percentage of protein, lipids, and carbohydrates in the diet of badger (Meles meles) populations across Europe. Ecol Res 26:487–495. https://doi.org/10.1007/s11284-011-0804-9 DOI
Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D (2022) Package “MASS”: support functions and datasets for venables and ripley’s MASS. R Package Version 7:3–29
Roslin T et al (2017) Higher predation risk for insect prey at low latitudes and elevations. Science 356:742–744. https://doi.org/10.1126/science.aaj1631 PubMed DOI
Růžička I (1972) Příspěvek ke květeně Českomoravské vysočiny II. [A contribution to the flora of the Bohemian-Moravian Highlands]. [In Czech]. Vlastivědný sborník Vysočiny. Oddíl věd přírodních: 53–65.
Seifert B (2018) The ants of central and north Europe. Lutra Germany
Similä M, Aapala K (2014) Ecological restoration in drained peatlands: best practices from Finland. Metsähallitus, Natural Heritage Services
Sipos J, Kindlmann P (2013) Effect of the canopy complexity of trees on the rate of predation of insects. J Appl Entomol 137:445–451. https://doi.org/10.1111/jen.12015 DOI
Sipos J, Drozdova M, Drozd P (2013) Assessment of trends in predation pressure on insects across temperate forest microhabitats. Agric Entomol 15:255–261. https://doi.org/10.1111/afe.12012 DOI
Skinner GJ (1980) The feeding-habits of the wood-ant, Formica-rufa (hymenoptera, formicidae), in limestone woodland in Northwest England. J Anim Ecol 49:417–433. https://doi.org/10.2307/4255 DOI
Skwarra E (1929) Formica fusca-picea Nyl. als Moorameise. Zool Anz 82:46–55
Spitzer K, Danks HV (2006) Insect biodiversity of boreal peat bogs. Annu Rev Entomol 51:137–161. https://doi.org/10.1146/annurev.ento.51.110104.151036 PubMed DOI
Spotti FA, Castracani C, Grasso DA, Mori A (2015) Daily activity patterns and food preferences in an alpine ant community. Ethol Ecol Evol 27:306–324. https://doi.org/10.1080/03949370.2014.947634 DOI
Stadler B, Dixon AFG (1998) Costs of ant attendance for aphids. J Anim Ecol 67:454–459. https://doi.org/10.1046/j.1365-2656.1998.00209.x DOI
Stein MB, Thorvilson HG, Johnson JW (1990) Seasonal-changes in bait preference by red imported fire ant, Solenopsis invicta (Hymenoptera, Formicidae). Fla Entomol 73:117–123. https://doi.org/10.2307/3495334 DOI
Stephens DW, Krebs JR (2019) Foraging Theory: Monographs in Behavior and Ecology. Princeton University Press, Princeton DOI
Sun Z, Jiang H (2017) Nutritive Evaluation of Earthworms as Human Food. In: Mikkola H (ed) Future foods. INTECH, Croatia, pp 127–142
Sutherland WJ et al (2013) Identification of 100 fundamental ecological questions. J Ecol 101:58–67. https://doi.org/10.1111/1365-2745.12025 DOI
Thompson JN et al (2001) Frontiers of ecology. Bioscience 51:15–24. https://doi.org/10.1641/0006-3568(2001)051[0015:foe]2.0.co;2 DOI
Toft S et al (2021) Contrasting patterns of food and macronutrient limitation in the field among co-existing omnivorous carnivores. Ecol Entomol 46:898–909. https://doi.org/10.1111/een.13026 DOI
Twardochleb LA, Treakle TC, Zarnetske PL (2020) Foraging strategy mediates ectotherm predator-prey responses to climate warming. Ecology. https://doi.org/10.1002/ecy.3146 PubMed DOI
von Liebig J (1840) Die organische Chemie in ihrer Anwendung auf Agricultur und Physiologie. Friedrich Vieweg und Sohn Publ, Co, Braunschweig, Germany
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York DOI
Wilder SM, Norris M, Lee RW, Raubenheimer D, Simpson SJ (2013) Arthropod food webs become increasingly lipid-limited at higher trophic levels. Ecol Lett 16:895–902. https://doi.org/10.1111/ele.12116 PubMed DOI
Zhigulskaya ZA, Shekhovtsov SV, Poluboyarova TV, Berman DI (2022) Formica picea and F candida (Hymenoptera: Formicidae): Synonyms or two species? Divers-Basel. https://doi.org/10.3390/d14080613 DOI
Zvereva EL, Kozlov MV (2023) Predation risk estimated on live and artificial insect prey follows different patterns. Ecology 104:13. https://doi.org/10.1002/ecy.3943 DOI