Significant impact of allochthonous nutrient loads on microarthropods in forest soils
Abstract
Aim of study: To investigate the impact of allochthonous material from piscivorous birds on forest soil microarthropod communities.
Area of study: Six study zones in the Curonian Spit peninsula (western Lithuania) were designated in Pinus sylvestris stands with nesting sites of the great cormorants, taking into account the relief and the duration of the ornithogenic impact.
Materials and methods: The total abundance of mites and Collembola and the species richness and diversity of Oribatida and Gamasina mites were assessed and compared.
Main results: The abundance of Collembola, Tarsonemidae and Acaridae mites positively correlated with ornithogenic activity, while Oribatida and Gamasina mites decreased significantly. The structure of microarthropod communities was similar in most of the studied zones, except for the active nesting zone and the abandoned part of the colony on the dune slope. The greatest species richness of Oribatida and Gamasina was found in the unaffected forest in the dune hollow, whereas the lowest value was found in the active nesting area and in the abandoned part of the colony on the dune slope. Of the environmental parameters studied, soil pH (r = - 0.725) and tree layer (r = 0.827) were those most significantly related to the changes of microarthropod communities.
Research highlights: We found that cormorant colonies have a strong impact on forest ecosystems and soil properties, leading to significant changes in soil microarthropod communities. Birds thus create a natural disturbance experiment that can help reveal the factors that determine the diversity and composition of natural microarthropod communities.
Downloads
References
Adamonytė G, Iršėnaitė R, Motiejūnaitė J, Matulevičiūtė D, Taraškevičius R, 2013. Myxomycetes in a forest affected by great cormorant colony: a case study in Western Lithuania. Fungal Divers 59(1): 131-146. https://doi.org/10.1007/s13225-012-0203-8
Bachrach U, 1957. The aerobic breakdown of uric acid by certain Pseudomonads. J Gen Microbiol 17: 1-11. https://doi.org/10.1099/00221287-17-1-1
Bakker MR, Brunner I, Ashwood F, Bjarnadottir B, Bolger T, Børja I et al., 2019. Belowground biodiversity relates positively to ecosystem services of European forests. Front For Glob Change 2: 6. https://doi.org/10.3389/ffgc.2019.00006
Balogh J, Balogh P, 1992. The oribatid mites genera of the world. Hungarian Natural History Museum, Budapest. vol. I: 263 p, vol. II: 375 p.
Bielska I, Paszewska H, 1997. Communities of moss mites (Acarida, Oribatida) on recultivated ash dumps from power plants. Pol Ecol Stud 21: 263-275.
Blasi S, Menta C, Balducci L, Conti FD, Petrini E, Piovesan G, 2013. Soil microarthropod communities from Mediterranean forest ecosystems in Central Italy under different disturbances. Environ Monit Assess 185: 1637-1655. https://doi.org/10.1007/s10661-012-2657-2
Braun-Blanquet J, 1964. Pflanzensoziologie. Grundzüge der Vegetationskunde. Springer, Wien-NY. 865 pp. https://doi.org/10.1007/978-3-7091-8110-2
Briones MJI, 2014. Soil fauna and soil functions: a jigsaw puzzle. Front Environ Sci 2: 7. https://doi.org/10.3389/fenvs.2014.00007
Brückner A, Raspotnig G, Wehner K, Meusinger R, Norton RA, Heethoff M, 2017. Storage and release of hydrogen cyanide in a chelicerate (Oribatula tibialis). P Nat Acad Sci 114(13): 3469-3472. https://doi.org/10.1073/pnas.1618327114
Bukantis A, 2013. Klimatas [Climate]. In: Lietuvos gamtinė geografija; Eidukevičienė M. (ed.). pp: 53-87. Klaipėdos universiteto leidykla, Klaipėda.
Cassagne N, Gauquelin T, Bal-Serin MC, Gers C, 2006. Endemic Collembola, privileged bioindicators of forest management. Pedobiologia 50: 127-134. https://doi.org/10.1016/j.pedobi.2005.10.002
Domínguez MT, Gutiérrez E, González-Domínguez B, Román M, Ávila AM, Ramo C et al., 2017. Impacts of protected colonial birds on soil microbial communities: when protection leads to degradation. Soil Biol Biochem 105: 59-70. https://doi.org/10.1016/j.soilbio.2016.11.007
Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB, 2012. Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Change Biol 18: 435-447. https://doi.org/10.1111/j.1365-2486.2011.02555.x
Ellis JC, 2005. Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol 181(2): 227-241. https://doi.org/10.1007/s11258-005-7147-y
Ghilarov MS, Krivolutsky DA, 1975. Identification of soil mites (Sarcoptiformes). Izd. Nauka, Moscow. 490 pp. [In Russian].
Ghilarov MS, Bregetova NG, 1977. A key to soil-dwelling mites (Mesostigmata). Russian Academy of Science, Leningrad. 717 pp. [In Russian]. Gudelis V, 1998. Lietuvos įjūris ir pajūris [Sea coast of Lithuania]. Lietuvos mokslas, Vilnius. 442 pp.
Hågvar S, 1982. Collembola in Norwegian coniferous forest soils: I. Relations to plant communities and soil fertility. Pedobiologia 24: 255-296.
Hågvar S, 1990. Reactions to soil acidification in microarthropods: Is competition a key factor? Biol Fertil Soils 9(2): 178-181. https://doi.org/10.1007/BF00335804
Hågvar S, Amundsen T, 1981. Effects of liming and artificial acid rain on the mite (Acari) fauna in coniferous forest. Oikos 37: 7-20. https://doi.org/10.2307/3544068
Hansen RA, 2000. Effects of habitat complexity and composition on a diverse litter microarthropod assemblage. Ecology 81(4): 1120-1132. https://doi.org/10.1890/0012-9658(2000)081[1120:EOHCAC]2.0.CO;2
Heneghan L, Bolger T, 1998. Soil microarthropod contribution to forest ecosystem processes: the importance of observational scale. Plant Soil 205: 113-124. https://doi.org/10.1023/A:1004374912571
Huhta V, Persson T, Setälä H, 1998. Functional implications of soil fauna diversity in boreal forests. Appl Soil Ecol 10: 277-288. https://doi.org/10.1016/S0929-1393(98)00126-7
Huhta V, Siira-Pietikäinen A, Penttinen R, 2012. Importance of dead wood for soil mite (Acarina) communities in boreal old-growth forests. Soil Organisms 84: 499-512.
Iršėnaitė R, Arslanova T, Kasparavičius J, Kutorga E, Markovskaja S, Matulevičiūtė D et al., 2019. Effects of a Great Cormorant colony on wood-inhabiting fungal communities in a coastal Scots pine forest. Fungal Ecol 41: 82-91. https://doi.org/10.1016/j.funeco.2019.03.010
Jončys F, Paulaitis A, 1987. Valstybinio Kuršių nerijos miško parko Juodkrantės girininkijos taksoraštis. Miškotvarka 1987 m. [Taxation report of Juodkrantė forest district, State Forest Park of Curonian Spit. Forest Management 1987]. Miškotvarkos Institutas, Kaunas. 172 pp.
Jucevica E, Melelis V, 2005. Long-term effects of climate warming on forest soil collembola. Acta Zool Lit 15(2): 124-126. https://doi.org/10.1080/13921657.2005.10512387
Kaliszewski M, Athias-Binche F, Lindquist EE, 1995. Parasitism and parasitoidism in Tarsonemina (Acari: Heterostigmata) and evolutionary considerations. Adv Parasit 35: 335-367. https://doi.org/10.1016/S0065-308X(08)60074-3
Kameda K, Koba K, Yoshimizu C, Fujiwara S, Hobara S, Koyama L et al., 2000. Nutrient flux from aquatic to terrestrial ecosystem mediated by the Great Cormorant. Sylvia 36 (Suppl.): 54-55.
Kataoka M, Nakamori T, 2020. Food preferences of Collembola for myxomycete plasmodia and plasmodium responses in the presence of Collembola. Fungal Ecol 47: 100965. https://doi.org/10.1016/j.funeco.2020.100965
Kitazawa Y, Kitazawa T, 1980. Influence of application of a fungicide, and insecticide, and compost upon soil biota community. Proc. 7th Intl Soil Zoology Colloquium: Soil Biology as Related to Land Use Practices, Syracuse, New York, 29 Jul-3 Aug 1979, pp: 94-98.
Klimaszyk P, Rzymski P, 2016. The complexity of ecological impacts induced by great cormorants. Hydrobiologia 771: 13-30. https://doi.org/10.1007/s10750-015-2618-1
Klimek A, Chachaj B, 2018. Colonization of hardwood and pine wood chips by mites (Acari), with particular reference to oribatid mites (Oribatida). Folia Forestalia Polonica, Series A - Forestry 60(1): 22-33. https://doi.org/10.2478/ffp-2018-0003
Klironomos JN, Kendrick B, 1995. Relationships among microarthropods, fungi, and their environment. Plant Soil 170: 183-197. https://doi.org/10.1007/BF02183066
Koehler HH, 1999. Predatory mites (Gamasina, Mesostigmata). Agric Ecosyst Environ 74: 395-410. https://doi.org/10.1016/B978-0-444-50019-9.50022-4
Kolb GS, Jerling L, Hambäck PA, 2010. The impact of cormorants on plant-arthropod food webs on their nesting islands. Ecosystems 13: 353-66. https://doi.org/10.1007/s10021-010-9323-8
Kolb GS, Palmborg C, Taylor AR, Bååth E, Hambäck PA, 2015. Effects of nesting cormorants (Phalacrocorax carbo) on soil chemistry, microbial communities and soil fauna. Ecosystems 18: 643-657. https://doi.org/10.1007/s10021-015-9853-1
Krivolutsky DA, Lebedeva NV, 2004. Oribatid mites (Oribatei) in bird feathers: Passeriformes. Acta Zool Lit 14: 19-37. https://doi.org/10.1080/13921657.2004.10512577
Kutorga E, Iršėnaitė R, Iznova T, Kasparavičius J, Markovskaja S, Motiejūnaitė J, 2013. Species diversity and composition of fungal communities in a Scots pine forest affected by the great cormorant colony. Acta Mycol 48: 173-188. https://doi.org/10.5586/am.2013.019
Lenoir L, Persson T, Bengtsson J, Wallander H, Wirén A, 2007. Bottom-up or top-down control in forest soil microcosms? Effects of soil fauna on fungal biomass and C/N mineralisation. Biol Fertil Soils 43: 281-294. https://doi.org/10.1007/s00374-006-0103-8
Liiri M, Setälä H, Haimi J, Pennanen T, Fritze H, 2002. Relationship between soil microarthropod species diversity and plant growth does not change when the system is disturbed. Oikos 96: 137-149. https://doi.org/10.1034/j.1600-0706.2002.960115.x
Lindo Z, Visser S, 2004. Forest floor microarthropod abundance and oribatid mite (Acari: Oribatida) composition following partial and clear-cut harvesting in the mixedwood boreal forest. Can J Forest Res 34: 998-1006. https://doi.org/10.1139/x03-284
Manu M, Iordache V, Bacila RI, Bodescu F, Onete M, 2016. The influence of environmental variables on soil mite communities (Acari: Mesostigmata) from overgrazed grassland ecosystems - Romania. Ital J Zool 83(1): 89-97. https://doi.org/10.1080/11250003.2015.1091897
Matulevičiūtė D, Motiejūnaitė J, Uogintas D, Taraškevičius R, Dagys M, Rašomavičius V, 2018. Decline of a protected coastal pine forest under impact of a colony of great cormorants and the rate of vegetation change under ornithogenic influence. Silva Fenn 52 (2): 131-146. https://doi.org/10.14214/sf.7699
McCune B, Grace JB, 2002. Analysis of ecological communities. MjM Software Design, Oregon, USA, 304 p.
McCune B, Mefford MJ, 2011. PC-ORD. Multivariate analysis of ecological data. Version 6. Gleneden Beach, Oregon, MjM Software.
Meehan ML, Barreto C, Turnbull MS, Bradley RL, Bellenger JP, Darnajoux R, Lindo Z, 2020. Response of soil fauna to simulated global change factors depends on ambient climate conditions. Pedobiologia 83: 150672. https://doi.org/10.1016/j.pedobi.2020.150672
Meloni F, Civieta BF, Zaragoza JA, Moraza ML, Bautista S, 2020. Vegetation pattern modulates ground arthropod diversity in semi-arid mediterranean steppes. Insects 11(1): 59. https://doi.org/10.3390/insects11010059
Morkūnaitė R, Baužienė I, Česnulevičius A, 2011. Parabolic dunes and soils of the Curonian Spit, south-eastern Baltic Sea coast. Baltica 24: 95-106.
Motiejūnaitė J, Kačergius A, Kasparavičius J, Taraškevičius R, Matulevičiūtė D, Iršėnaitė R, 2021. Response of ectomycorrhizal and other Pinus sylvestris root-associated fungi to the load of allochtonous material from a great cormorant colony. Mycorrhiza 31: 471-481. https://doi.org/10.1007/s00572-021-01034-5
Niogret J, Nicot A, Bertrand M, 2007. Two new species of Macrocheles from France (Mesostigmata: Macrochelidae). Acarologia 47: 115-120.
Osono T, 2012. Excess supply of nutrients, fungal community, and plant litter decomposition: a case study of avian-derived excreta deposition in conifer plantations. In: International Perspectives on Global Environmental Change, Young SS, Silvern SE (eds). In Tech. eBook. https://doi.org/10.5772/26491
Osono T, Hobara S, Fujiwara S, Koba K, Kameda K, 2002. Abundance, diversity, and species composition of fungal communities in a temperate forest affected by excreta of the great cormorant Phalacrocorax carbo. Soil Biol Biochem 34: 1537-1547. https://doi.org/10.1016/S0038-0717(02)00123-2
Parisi V, Menta C, Gardi C, Jacomini C, Mozzanica E, 2005. Microarthropod communities as a tool to assess soil quality and biodiversity: a new approach in Italy. Agr Ecosyst Environ 105(1-2): 323-333. https://doi.org/10.1016/j.agee.2004.02.002
Peyrat J, 2007. Development, properties and classification of dune soils in the Curonian Spit National Park, Russian part. Geologija 59: 59-64.
Petersen H, Luxton M, 1982. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39: 287-388. https://doi.org/10.2307/3544689
Ponge JF, Gillet S, Dubs F, Fédorof E, Haese L, Sousa J, Lavelle P, 2003. Collembolan communities as bioindicators of land use intensification. Soil Biol Biochem 35 (6): 813-826. https://doi.org/10.1016/S0038-0717(03)00108-1
Proctor H, Owens I, 2000. Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 15(9): 358-364. https://doi.org/10.1016/S0169-5347(00)01924-8
Reis F, Carvalho F, Martins da Silva P, Mendes S, Santos SAP, Sousa JP, 2016. The use of a functional approach as surrogate of Collembola species richness in European perennial crops and forests. Ecol Indic 61: 676-682. https://doi.org/10.1016/j.ecolind.2015.10.019
Ruf A, Beck L, 2005. The use of predatory soil mites in ecological soil classification and assessment concepts, with perspectives for oribatid mites. Ecotox Environ Safe 62(2): 290-299. https://doi.org/10.1016/j.ecoenv.2005.03.029
Sanchez-Piñero F, Polis GA, 2000. Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81: 3117-3132. https://doi.org/10.1890/0012-9658(2000)081[3117:BUDOAI]2.0.CO;2
Schneider K, Migge S, Norton RA, Scheu S, Langel R, Reineking A, Maraun M. 2004. Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36: 1769-1774. https://doi.org/10.1016/j.soilbio.2004.04.033
Seniczak S, Norton RA, Seniczak A, 2009. Morphology of Eniochthonius minutissimus (Berlese, 1904) and Hypochthonius rufulus C. L. Koch, 1835 (Acari: Oribatida: Hypochthonioidea). Annales Zoologici 59(3): 373-386. https://doi.org/10.3161/000345409X476440
Shannon CE, 1948. A mathematical theory of communication. Bell Syst Tech J 27: 379-423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Skubała P, Kafel A, 2004. Oribatid mite communities and metal bioaccumulation in oribatid species (Acari, Oribatida) along the heavy metal gradient in forest ecosystems. Environ Pollut 132(1): 51-60. https://doi.org/10.1016/j.envpol.2004.03.025
Tousignat S, Coderre D, 1992. Niche partitioning by soil mites in a recent hardwood plantation in Southern Quebec, Canada. Pedobiologia 36: 287-294.
Towns DR, Wardle DA, Mulder CPH, Yeates GW, Fitzgerald BM, Parrish GR, Bellingham PJ, Bonner KI, 2009. Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118: 420-430. https://doi.org/10.1111/j.1600-0706.2008.17186.x
Urbanovičová V, Miklisová D, Kováč L, 2014. Forest disturbance enhanced the activity of epedaphic collembola in windthrown stands of the High Tatra mountains. J Mt Sci 11: 449-463. https://doi.org/10.1007/s11629-013-2736-z
Zmudczyńska K, Olejniczak I, Zwolicki A, Iliszko L, Convey P, Stempniewcz L, 2012. Influence of allochtonous nutrients delivered by colonial seabirds on soil collembolan communities on Spitsbergen. Polar Biol 35: 1233-1245. https://doi.org/10.1007/s00300-012-1169-4
Žydelis R, Gražulevičius G, Zarankaitė J, Mečionis R, Mačiulis M, 2002. Expansion of the Cormorant (Phalacrocorax carbo sinensis) population in western Lithuania. Acta Zool Lit 12: 283-287. https://doi.org/10.1080/13921657.2002.10512515
Copyright (c) 2022 CSIC_INIA
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.
