Above- and belowground habitat complexity created by emergent and submerged vegetation drives the structure of benthic assemblages

Pawlikowski, Krzysztof; Kornijów, Ryszard

doi:10.1016/j.oceano.2022.10.002

Artykuł - szczegóły

Tytuł artykułu

Above- and belowground habitat complexity created by emergent and submerged vegetation drives the structure of benthic assemblages

Autorzy

Pawlikowski Krzysztof , Kornijów Ryszard

Wybrane pełne teksty z tego czasopisma

Identyfikatory

DOI

10.1016/j.oceano.2022.10.002

Warianty tytułu

Języki publikacji

Abstrakty

The contrast in habitat complexity between emergent (EMV) and submerged vegetation (SUV) zones in aquatic ecosystems results from the differences in the structure of plant above- and belowground parts, subject to seasonal changes. Comparative studies on the influence of habitat complexity created by vegetation on benthic macroinvertebrates in coastal areas are scarce. In order to fill this knowledge gap, we performed a study on a seasonal basis in the brackish Vistula Lagoon (southern Baltic Sea) in two zones: EMV, dominated by a dense belt of Phragmites australis (Cav.) Trin. ex Steud, and SUV, with scattered stands of Potamogeton perfoliatus L. We assumed the following: i. Species richness, diversity, and density of invertebrates are higher in the EMV zone due to greater and less seasonally variable structural complexity than in the SUV zone, ii. High belowground complexity in the EMV zone due to the presence of the rhizome/root matrix, much more robust and denser than in the SUV zone limits the vertical distribution of macroinvertebrates. Both hypotheses were supported. Overall, our results pointing to higher animal diversity and density in more complex aquatic habitats are consistent with other studies, inferred mostly from comparative surveys of bare bottom and that covered with submerged vegetation. The results of this study highlight potentially far-reaching implications for benthic invertebrate fauna and their role in the aquatic ecosystem in the context of increasingly rapid loss of aquatic vegetation due to multiple anthropogenic stressors.

Słowa kluczowe

Vistula Lagoon littoral trophic guilds macrophytes vertical distribution

Wydawca

Polish Academy of Sciences, Institute of Oceanology
Elsevier

Czasopismo

Oceanologia

Rocznik

2023

Tom

Vol. 65 (2)

Strony

358--370

Opis fizyczny

Bibliogr. 82 poz., map., rys., tab., wykr.

Twórcy

autor

Pawlikowski Krzysztof

kpawlikowski@mir.gdynia.pl

National Marine Fisheries Research Institute, Gdynia, Poland

https://orcid.org/0000-0002-9855-4399

autor

Kornijów Ryszard

National Marine Fisheries Research Institute, Gdynia, Poland

Bibliografia

1. Armitage, P.D., Cranston, P.S., Pinder, L.C.V., 1995. The Chironomidae. Biology and ecology of non-biting midges. Chapman and Hall, Londyn-Madryt, 447 pp. https://doi.org/10.1007/978-94-011-0715-0
2. Blott, S.J., Pye, K., 2001. GRADISTAT: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surf. Proc. Land. 26, 1237-1248. https://doi.org/10.1002/esp.261
3. Boström, C., Bonsdorff, E., 1997. Community structure and spatial variation of benthic invertebrates associated with Zostera marina (L) beds in the northern Baltic Sea. J. Sea Res. 37, 153-166. https://doi.org/10.1016/S1385-1101(96)00007-X
4. Boström, C., Bonsdorff, E., 2000. Zoobenthic community establishment and habitat complexity - the importance of seagrass shoot-density, morphology and physical disturbance for faunal recruitment. Mar. Ecol. Prog. Ser. 205, 123-138. https://doi.org/10.3354/meps205123
5. Brucet, S., Boix, D., Nathansen, L.W., Quintana, X.D., Jensen, E., Balayla, D., Meerhoff, M., Jeppesen, E., 2012. Effects of temperature, salinity and fish in structuring the macroinvertebrate community in shallow lakes: Implications for effects of climate change. Plos One 7. https://doi.org/10.1371/journal.pone.0030877
6. Caffrey, J.M., Kemp, W.M., 1992. Influence of the submersed plant, Potamogeton perfoliatus, on nitrogen cycling in estuarine sediments. Limnol. Oceanogr. 37, 1483-1495. https://doi.org/10.4319/lo.1992.37.7.1483
7. Cardoso, I., Granadeiro, J.P., Cabral, H., 2010. Benthic macroinvertebrates’ vertical distribution in the Tagus estuary (Portugal): The influence of tidal cycle. Estuar. Coast. Shelf S. 86, 580-586. https://doi.org/10.1016/j.ecss.2009.11.024
8. Carpenter, S.R., Lodge, D.M., 1986. Effects of submersed macrophytes on ecosystem processes. Aquat. Bot. 26, 341-370. https://doi.org/10.1016/0304-3770(86)90031-8
9. Como, S., Magni, P., Baroli, M., Casu, D., De Falco, G., Floris, A., 2008. Comparative analysis of macrofaunal species richness and composition in Posidonia oceanica, Cymodocea nodosa and leaf litter beds. Mar. Biol. 153, 1087-1101. https://doi.org/10.1007/s00227-007-0881-z
10. Dauer, D.M., Ewing, R.M., Rodi, A.J., 1987. Macrobenthic distribution within the sediment along an estuarine salinity gradient. Int. Rev. Ges. Hydrobiol. 72, 529-538. https://doi.org/10.1002/iroh.19870720502
11. Davis, R.B., 1974. Stratigraphic effects of tubificids in profundal lake sediments. Limnol. Oceanogr. 19, 466-488. https://doi.org/10.4319/lo.1974.19.3.0466
12. Diehl, S., Kornijów, R., 1998. Influence of submerged macrophytes on trophic interactions among fish and macroinvertebrates. In: Jeppesen, E., Søndergaard, M., Søndergaard, M., Christoffersen, M. (Eds.), The structuring role of submerged macrophytes in lakes. Ecol. Stud 131. Springer, New York, 24-46. https://doi.org/10.1007/978-1-4612-0695-8_2
13. Donnelly, A.P., Herbert, R.A., 1999. Bacterial interactions in the rhizosphere of seagrass communities in shallow coastal lagoons. J. Appl. Microbiol. 85, 151S-160S. https://doi.org/10.1111/j.1365-2672.1998.tb05294.x
14. Evans, C.A., O’Reilly, J.E., 1983. A handbook for the measurement of chlorophyll a in netplankton and nannoplankton. In: Biomass handbook No.9. SCAR/SCOR/IABO/ACMRR Group of specialists on living resources of the southern oceans. SCAR, 44 pp.
15. Fredriksen, S., De Backer, A., Bostrom, C., Christie, H., 2010. Infauna from Zostera marina L. meadows in Norway. Differences in vegetated and unvegetated areas. Mar. Biol. Res. 6, 189-200. https://doi.org/10.1080/17451000903042461
16. González-Ortiz, V., Alcazar, P., Vergara, J.J., Pérez-Lloréns, J., Brun, F.G., 2014. Effects of two antagonistic ecosystem engineers on infaunal diversity. Estuar. Coast. Shelf S. 139, 20-26. https://doi.org/10.1016/j.ecss.2013.12.015
17. González-Ortiz, V., Egea, L.G., Jiménez-Ramos, R., Moreno-Marin, F., Pérez-Lloréns, J., Bouma, T., Brun, F., 2016. Submerged vegetation complexity modifies benthic infauna communities: the hidden role of the belowground system. Mar. Ecol.-Evol. Persp. 37, 543-552. https://doi.org/10.1111/maec.12292
18. Gonzalez, M.J., Burkart, G.A., 2004. Effects of food type, habitat, and fish predation on the relative abundance of two amphipod species, Gammarus fasciatus and Echinogammarus ischnus. J. Great Lakes Res. 30, 100-113. https://doi.org/10.1016/s0380-1330(04)70333-0
19. Goshima, S., Peterson, C.H., 2012. Both below- and aboveground shoalgrass structure influence whelk predation on hard clams. Mar. Ecol. Prog. Ser. 451, 75-92. https://doi.org/10.3354/meps09587
20. Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379-391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
21. Gotelli, N.J., Entsminger, G.L., 2009. EcoSim: Null models software for ecology, Version 7, Acquired Intelligence Inc. & Kesey-Bear. http://www.uvm.edu/∼ngotelli/EcoSim/EcoSim.html.
22. Gotelli, N.J., Graves, G.R., 1996. Null models in ecology. Smithsonian Institution Press, Washington, D.C., 368 pp.
23. Holomuzki, J.R., Hoyle, J.D., 1990. Effect of predatory fish presence on habitat use and diel movement of the stream amphipod, Gammarus minus. Freshwater Biol 24, 509-517. https://doi.org/10.1111/j.1365-2427.1990.tb00728.x
24. Hoffman, C.E., 1940. The relation of Donacia larvae (Chrysomelidae: Coleophera) to dissolved oxygen. Ecol. Evol. 21, 176-183. https://doi.org/10.2307/1930484
25. Huang, R., Zeng, J., Zhao, D.Y., Cook, K.V., Hambright, K.D., Yu, Z.B., 2020. Sediment microbiomes associated with the rhizosphere of emergent macrophytes in a shallow, subtropical lake. Limnol. Oceanogr. 65, S38-S48. https://doi.org/10.1002/lno.11325
26. James, M.R., Weatherhead, M., Stanger, C., Graynoth, E., 1998. Macroinvertebrate distribution in the littoral zone of Lake Coleridge, South Island, New Zealand - effects of habitat stability, wind exposure, and macrophytes. New Zeal. J. Mar. Fresh. 32, 287-305. https://doi.org/10.1080/00288330.1998.9516826
27. Janas, U., Kendzierska, H., 2014. Benthic non-indigenous species among indigenous species and their habitat preferences in Puck Bay (southern Baltic Sea). Oceanologia 56 (3), 603-628. https://doi.org/10.5697/oc.56-3.603
28. Jeppesen, E., Søndergaard, M., Søndergaard, M., Christoffersen, K., 1998. The structuring role of submerged macrophytes in lakes. Springer, New York, 131 pp.
29. Kajak, Z., 1988. Considerations on benthos abundance in fresh-waters, its factors and mechanisms. Int. Rev. Ges. Hydrobiol. 73, 5-19. https://doi.org/10.1002/iroh.19880730103
30. Kajak, Z., Dusoge, K., 1971. The regularities of vertical distribution of benthos in bottom sediments of three Masurian lakes. Ekol. Pol. 19, 485-499.
31. Kajak, Z., Warda, J., 1970. Food conditions for. Iarvae of Chironomidae in various layers of bottom sediments. Bull. Acad. Pol. Sci. 18, 193-196.
32. Kangur, K., Timm, H., Timm, T., Timm, V., 1998. Long-term changes in the macrozoobenthos of Lake Võrtsjärv. Limnologica 28, 75-83.
33. Kemp, W.M., Lewis, M.R., Jones, T.W., 1986. Comparison of methods for measuring production by the submersed macrophyte, Potamogeton perfoliatus L. Limnol. Oceanogr. 31, 1322-1334. https://doi.org/10.4319/lo.1986.31.6.1322
34. Kemp, W.M., Murray, L., 1986. Oxygen release from roots of the submersed macrophyte Potamogeton perfoliatus L.: Regulating factors and ecological implications. Aquat. Bot. 26, 271-283. https://doi.org/10.1016/0304-3770(86)90027-6
35. Kornijów, R., 1997. The impact of predation by perch on the size-structure of Chironomus larvae - The role of vertical distribution of the prey in the bottom sediments, and habitat complexity. Hydrobiologia 342, 207-213. https://doi.org/10.1023/A:1017067621668
36. Kornijów, R., 2013. A new sediment slicer for rapid sectioning of the uppermost sediment cores from marine and freshwater habitats. J. Paleolimnol. 49, 301-304. https://doi.org/10.1007/s10933-012-9655-9
37. Kornijów, R., 2018. Ecosystem of the Polish part of the Vistula Lagoon from the perspective of alternative stable states concept, with implications for management issues. Oceanologia 60 (3), 390-404. https://doi.org/10.1016/j.oceano.2018.02.004
38. Kornijów, R., Dukowska, M., Leszczynska, J., Smith, C., Jeppesen, E., Hansson, L.A., Ketola, M., Irvine, K., Noges, T., Sahuquillo, M., Miracle, M.R., Gross, E., Kairesalo, T., van Donk, E., de Eyto, E., Garcia-Criado, F., Grzybkowska, M., Moss, B., 2021a. Distribution patterns of epiphytic reed-associated macroinvertebrate communities across European shallow lakes. Sci. Total Environ. 760. https://doi.org/10.1016/j.scitotenv.2020.144117
39. Kornijów, R., Gulati, R.D., 1992. Macrofauna and its ecology in Lake Zwemlust, after biomanipulation. I. Bottom fauna. Arch. Hydrobiol. 123, 337-347.
40. Kornijów, R., Moss, B., 1998. Vertical distribution of in-benthos in relation to fish and floating-leaved macrophyte populations, in: Jeppesen, E., Søndergaard, M., Søndergaard, M., Christoffersen, K. (Eds.), The structuring role of submerged macrophytes in lakes. Ecol. Stud 131. Springer, New York, 227-232. https://doi.org/10.1007/978-1-4612-0695-8_12
41. Kornijów, R., Pawlikowski, K., Bł˛edzki, L.A., Drgas, A., Piwosz, K., Ameryk, A., Całkiewicz, J., 2021b. Co-occurrence and potential resource partitioning between oligochaetes and chironomid larvae in a sediment depth gradient. Aquat. Sci. 83 (51), 1-10. https://doi.org/10.1007/s00027-021-00800-z
42. Kristensen, E., Penha-Lopes, G., Delefosse, M., Valdemarsen, T., Quintana, C.O., Banta, G.T., 2012. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar. Ecol. Prog. Ser. 446, 285-302. https://doi.org/10.3354/meps09506
43. Lellak, J., 1965. The food supply as a factor regulating the population dynamics of bottom animals. Verh. Int. Ver. Theor. Angew. Limnol. 13, 128-138.
44. Levin, S.A., 1992. The problem of pattern and scale in ecology. Ecology 73, 1943-1967. https://doi.org/10.2307/1941447
45. Liu, W.Z., Jiang, X.L., Zhang, Q.F., Li, F., Liu, G.H., 2018. Has submerged vegetation loss altered sediment denitrification, N2 O production, and denitrifying microbial communities in subtropical lakes? Global Biogeochem. Cy. 32, 1195-1207. https://doi.org/10.1029/2018gb005978
46. Magni, P., Como, S., Kamijo, A., Montani, S., 2017. Effects of Zostera marina on the patterns of spatial distribution of sediments and macrozoobenthos in the boreal lagoon of Furen (Hokkaido, Japan). Mar. Environ. Res. 131, 90-102. https://doi.org/10.1016/j.marenvres.2017.09.013
47. Meerhoff, M., González-Sagrario, M.A., 2021. Habitat complexity in shallow lakes and ponds: importance, threats, and potential for restoration. Hydrobiologia https://doi.org/10.1007/s10750-021-04771-y
48. Mermillod-Blondin, F., 2011. The functional significance of bioturbation and biodeposition on biogeochemical processes at the water-sediment interface in freshwater and marine ecosystems. J. N. Am. Benthol. Soc. 30, 770-778. https://doi.org/10.1899/10-121.1
49. Meyerson, L.A., Cronin, J.T., Pysek, P., 2016. Phragmites australis as a model organism for studying plant invasions. Biol. Invasions 18, 2421-2431. https://doi.org/10.1007/s10530-016-1132-3
50. Milbrink, G., 1973. On the vertical distribution of oligochaetes in lake sediments. Institute for Freshwater Research, Drottningholm, 34-50.
51. Morris, K., Bailey, P.C., Boon, P.I., Hughes, L., 2003. Alternative stable states in the aquatic vegetation of shallow urban lakes. II. Catastrophic loss of aquatic plants consequent to nutrient enrichment. Mar. Freshwater Res. 54, 201-215. https://doi.org/10.1071/mf02003
52. Mrozińska, N., Glińska-Lewczuk, K., Obolewski, K., 2021. Salinity as a key factor on the fenthic fauna diversity in the coastal lakes. Animals 11, 3039. https://doi.org/10.3390/ani11113039
53. Newrkla, P., Wijegoonawardana, N., 1987. Vertical distribution and abundance of benthic invertebrates in profundal sediments of Mondsee, with special reference to Oligochaetes. Hydrobiologia 155, 227-234. https://doi.org/10.1007/Bf00025655
54. Orth, R.J., 1977. The importance of sediment stability in seagrass communities. In: Coull, B.C. (Ed.), Ecology of Marine Benthos. University of South Carolina Press, Columbia, 281-300.
55. Ostendorp, W., 1989. Die-back’ of reeds in Europe: a critical review of literature. Aquat. Bot. 35, 5-26. https://doi.org/10.1016/0304-3770(89)90063-6
56. Ozimek, T., Prejs, A., Prejs, K., 1976. Biomass and distribution of underground parts of Potamogeton perfoliatus L. and P. lucens L. in Mikołajskie Lake. Poland. Aquat. Bot. 2, 309-316. https://doi.org/10.1016/0304-3770(76)90028-0
57. Pawlikowski, K., Kornijów, R., 2019. Role of macrophytes in structuring littoral habitats in the Vistula Lagoon (southern Baltic Sea). Oceanologia 61 (1), 26-37. https://doi.org/10.1016/j.oceano.2018.05.003
58. Persson, A., Svensson, J.M., 2006. Vertical distribution of benthic community responses to fish predators, and effects on algae and suspended material. Aquat. Ecol. 40, 85-95. https://doi.org/10.1007/s10452-005-9014-2
59. Peterson, C.H., 1982. Clam predation by whelks (Busycon spp.): Experimental tests of the importance of prey size, prey density, and seagrass cover. Mar. Biol. 66, 159-170. https://doi.org/10.1007/Bf00397189
60. Phillips, G., Willby, N., Moss, B., 2016. Submerged macrophyte decline in shallow lakes: What have we learnt in the last forty years? Aquat. Bot. 135, 37-45. https://doi.org/10.1016/j.aquabot.2016.04.004
61. Pieczyńska, E., 1993. Detritus and nutrient dynamics in the shore zone of lakes - a review. Hydrobiologia 251, 49-58. https://doi.org/10.1007/Bf00007164
62. PRIMER-E Ltd, 2007. PRIMER 6 software. 6.1.9. http://www.primer-e.com
63. Rodil, I.F., Cividanes, S., Lastra, M., Lopez, J., 2008. Seasonal variability in the vertical distribution of benthic macrofauna and sedimentary organic matter in an estuarine beach (NW spain). Estuar. Coast. 31, 382-395. https://doi.org/10.1007/s12237-007-9017-4
64. Rodil, I.F., Lohrer, A.M., Attard, K.M., Hewitt, J.E., Thrush, S.F., Norkko, A., 2021. Macrofauna communities across a seascape of seagrass meadows: environmental drivers, biodiversity patterns and conservation implications. Biodivers. Conserv. 30, 3023-3043. https://doi.org/10.1007/s10531-021-02234-3
65. Ságová-Marečková, M., 2002. Distribution of benthic macroinvertebrates in relationship to plant roots, sediment type and spatial scale in fishponds and slow streams. Arch. Hydrobiol. 156, 63-81. https://doi.org/10.1127/0003- 9136/2002/0156- 0063
66. Ságová, M., Adams, M.S., Butler, M.G., 1993. Relationship between plant-roots and benthic animals in three sediment types of a dimictic mesotrophic lake. Arch. Hydrobiol. 128, 423-436.
67. Siebert, T., Branch, G.M., 2005. Interactions between Zostera capensis, Callianassa kraussi and Upogebia africana: deductions from field surveys in Langebaan Lagoon, South Africa. Afr. J. Mar. Sci. 27, 345-356. https://doi.org/10.2989/18142320509504094
68. Siebert, T., Branch, G.M., 2007. Influences of biological interactions on community structure within seagrass beds and sandprawn-dominated sandflats. J. Exp. Mar. Biol. Ecol. 340, 11-24. https://doi.org/10.1016/j.jembe.2006.08.007
69. StatSoft, 2011. Statistica software version 10. StatSoft Inc https://doi.org/http://www.statsoft.com
70. Sueiro, M.C., Bortolus, A., Schwindt, E., 2011. Habitat complexity and community composition: relationships between different ecosystem engineers and the associated macroinvertebrate assemblages. Helgoland Mar. Res. 65, 467-477. https://doi.org/10.1007/s10152-010-0236-x
71. Takamura, N., Ito, T., Ueno, R., Ohtaka, A., Wakana, I., Nakagawa, M., Ueno, Y., Nakajima, H., 2009. Environmental gradients determining the distribution of benthic macroinvertebrates in Lake Takkobu, Kushiro wetland, northern Japan. Ecol. Res. 24, 371-381. https://doi.org/10.1007/s11284-008-0514-0
72. Touhami, F., Bazairi, H., Badaoui, B., Benhoussa, A., 2018. Vertical distribution of benthic macrofauna in intertidal habitats frequented by shorebirds at Merja Zerga Lagoon. Thalassas 34, 255-265. https://doi.org/10.1007/s41208-017-0059-5
73. Van de Bund, W.J., Groenendijk, D., 1994. Seasonal dynamics and burrowing of littoral Chironomid larvae in relation to competition and predation. Arch. Hydrobiol. 132, 213-225.
74. Vaughn, C.C., 1982. Distribution of chironomids in the Littoral-Zone of Lake Texoma, Oklahoma and Texas. Hydrobiologia 89, 177-188. https://doi.org/10.1007/Bf00006170
75. Vidal, N., Yu, J.L., Gutierrez, M.F., de Mello, F.T., Tavsanoglu, U.N., Cakiroglu, A.I., He, H., Meerhoff, M., Brucet, S., Liu, Z.W., Jeppesen, E., 2021. Salinity shapes food webs of lakes in semiarid climate zones: a stable isotope approach. Inland Waters 11, 445-456. https://doi.org/10.1080/20442041.2020.1859290
76. Webster, P.J., Rowden, A.A., Attrill, M.J., 1998. Effect of shoot density on the infaunal macro-invertebrate community within a zostera marina seagrass bed. Estuar. Coast. Shelf Sci. 47, 351-357. https://doi.org/10.1006/ecss.1998.0358
77. Weisner, S.E.B., Strand, J.A., 1996. Rhizome architecture in Phragmites australis in relation to water depth: Implications for within-plant oxygen transport distances. Folia Geobot. Phytotx. 31, 91-97. https://doi.org/10.1007/bf02803998
78. Whitlatch, R.B., 1980. Patterns of resource utilization and coexistence in marine inter-tidal deposit-feeding communities. J. Mar. Res. 38, 743-765.
79. Wolfer, S.R., Straile, D., 2004. Spatio-temporal dynamics and plasticity of clonal architecture in Potamogeton perfoliatus. Aquat. Bot. 78, 307-318. https://doi.org/10.1016/j.aquabot.2003.11.005
80. Wolnomiejski, N., 1994. Ecological study on muddy bottom macrofauna of the Szczecin Lagoon (1982-1992). Studia i Materiały, Marine Fisheries Institute, Gdynia ser. A, 31, Gdynia, 126 pp., (in Polish).
81. Wolnomiejski, N., Furyk, A., 1968. The vertical distribution of the bottom fauna in the sediments of the littoral zone of Jeziorak Lake. Zesz. Nauk. UMK w Toruniu, Nauki Mat.-Przyr., Prace Stacji Limnologicznej w Iławie 20, 31-45.
82. Zhang, Y.L., Jeppesen, E., Liu, X.H., Qin, B.Q., Shi, K., Zhou, Y.Q., Thomaz, S.M., Deng, J.M., 2017. Global loss of aquatic vegetation in lakes. Earth-Sci. Rev. 173, 259-265. https://doi.org/10.1016/j.earscirev.2017.08.013

Uwagi

Opracowanie rekordu ze środków MEiN, umowa nr SONP/SP/546092/2022 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2022-2023). (PL)

Typ dokumentu

Bibliografia

Identyfikator YADDA

bwmeta1.element.baztech-f6892f7e-3da1-428f-804b-912209f48f4a