Abstract
There are surprisingly few field studies on the role of invasive species on parasite infection patterns in native hosts. We investigated the role of invasive Pacific oysters (Magallana gigas) in determining parasite infection levels in native blue mussels (Mytilus edulis) in relation to other environmental and biotic factors. Using hierarchical field sampling covering three spatial scales along a large intertidal ecosystem (European Wadden Sea), we found strong spatial differences in infection levels of five parasite species associated with mussels and oysters. We applied mixed models to analyse the associations between parasite prevalence and abundance in mussels and oysters, and 12 biological and environmental factors. For each parasite–host relationship, an optimal model (either a null, one-factor or two-factor model) was selected based on AIC scores. We found that the density of invasive oysters contributed to three of the 12 models. Other biological factors such as host size (six models), and the density of target or alternative host species (five models) contributed more frequently to the best models. Furthermore, for parasite species infecting both mussels and oysters, parasite population densities were higher in native mussels, attributed to the higher densities of mussels. Our results indicate that invasive species can affect parasite infection patterns in native species in the field, but that their relative contribution may be further mediated by other biological and environmental parameters. These results stress the usefulness of large-scale field studies for detailed assessments of the mechanisms underlying the impacts of invasive species on native host communities.
References
Ambariyanto, Seed R (1991) The infestation of Mytilus edulis Linnaeus by Polydora ciliata (Johnston) in the Conwy estuary, North Wales. J Molluscan Stud 57:413–424. https://doi.org/10.1093/mollus/57.4.413
Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc Lond B 265:1283–1289. https://doi.org/10.1098/rspb.1998.0431
Barton K (2018) MuMIn: multi-model inference. R package version 1.40.4 https://CRAN.R-project.org/package=MuMIn. Accessed 16 Feb 2019
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323. https://doi.org/10.1016/s0308-597x(03)00041-1
Bolster GC (1954) The biology and dispersal of Mytilicola intestinalis Steuer, a copepod parasite of mussels. Fish In Min Fish Food 18:1–30
Brenner M, Broeg K, Frickenhaus S, Buck BH, Koehler A (2014) Multi-biomarker approach using the blue mussel (Mytilus edulis L.) to assess the quality of marine environments: season and habitat-related impacts. Mar Environ Res 95:13–27. https://doi.org/10.1016/j.marenvres.2013.12.009
Burchard H, Bolding K (2002) GETM (2002) A general estuarine transport model. scientific documentation. Technical report. EUR 20253 EN European Commission
Buschbaum C, Buschbaum G, Schrey I, Thieltges DW (2007) Shell-boring polychaetes affect gastropod shell strength and crab predation. Mar Ecol Prog Ser 329:123–130. https://doi.org/10.3354/meps329123
Buschbaum C, Cornelius A, Goedknegt MA (2016) Deeply hidden inside introduced biogenic structures—Pacific oyster reefs reduce detrimental barnacle overgrowth on native blue mussels. J Sea Res 117:20–26. https://doi.org/10.1016/j.seares.2016.09.002
Bush AO, Lafferty KD, Lotz JM, Shostak AW et al (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227
Byers JE, Blakeslee AMH, Linder E, Cooper AB, Maguire T (2008) Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89:439–451. https://doi.org/10.1890/06-1036.1
Caspers H (1939) Über Vorkommen und Metamorphose van Mytilicola intestinalis Steuer (Copepoda paras.) in der südlichen Nordsee. Zool Anz 126:161–171
Catherine M, Blateau D, Mazurié J, Le Bec C (1990) Anomalies des coquilles d’ huîtres creuses Crassostrea gigas observées sur le littoral français en mai-juin 1989, dues au ver Polydora et aux peintures antisalissures. Rapports Internes de la Direction des Ressources Vivantes de I’Ifremer. RIDRV 90.22-CSRU-RA/Nantes-La Trinite sur Mer
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449. https://doi.org/10.1126/science.287.5452.443
Davey JT, Gee JM (1976) The occurrence of Mytilicola intestinalis STEUER, an intestinal copepod parasite of Mytilus, in the South-West of England. J Mar Biol Assoc UK 56:85–94. https://doi.org/10.1017/s0025315400020452
Drinkwaard AC (1999) Introductions and developments of oysters in the North Sea area: a review. Helgol Mer Res 52:301–308. https://doi.org/10.1007/bf02908904
Elsner NO, Jacobsen S, Thieltges DW, Reise K (2011) Alien parasitic copepods in mussels and oysters of the Wadden Sea. Helgol Mar Res 65:299–307. https://doi.org/10.1007/s10152-010-0223-2
Eschweiler N, Christensen HT (2011) Trade-off between increased survival and reduced growth for blue mussels living on Pacific oyster reefs. J Exp Mar Biol Ecol 403:90–95. https://doi.org/10.1016/j.jembe.2011.04.010
Feis ME (2018) Host-parasite co-evolution and co-infection of invasive parasitic Mytilicola copepods in blue mussel hosts. Ph.D. dissertation, Faculty of Mathematics and Natural Sciences, Kiel University, Kiel, Germany
Fingerut JT, Zimmer CA, Zimmer RK (2003) Patterns and processes of larval emergence in an estuarine parasite system. Biol Bull 205:110–120. https://doi.org/10.2307/1543232
Folmer EO, Drent J, Troost K, Büttger H, Dankers N, Jansen J, van Stralen M, Millat G, Herlyn M, Philippart CJM (2014) Large-scale spatial dynamics of intertidal mussel (Mytilus edulis L.) bed coverage in the German and Dutch Wadden Sea. Ecosystems 17:550–566. https://doi.org/10.1007/s10021-013-9742-4
Folmer EO, van Beusekom JEE, Dolch T, Gräwe U, Katwijk MM, Kolbe K, Philippart CJM (2016) Consensus forecasting of intertidal seagrass habitat in the Wadden Sea. J Appl Ecol 53:1800–1813. https://doi.org/10.1111/1365-2664.12681
Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Method Softw 27:233–249. https://doi.org/10.1080/10556788.2011.597854
Galaktionov KV, Bustnes JO (1999) Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea. Dis Aquat Org 37:221–230. https://doi.org/10.3354/dao037221
Galaktionov KV, Bustnes JO, Bårdsen B-J, Wilson JG, Nikolaev KE, Sukhotin AA, Skírnisson Saville DH, Ivanov MV, Regel KV (2015) Factors influencing the distribution of trematode larvae in blue mussels Mytilus edulis in the North Atlantic and Arctic Oceans. Mar Biol 162:193–206. https://doi.org/10.1007/s00227-014-2586-4
Gee JM, Davey JT (1986) Experimental studies on the infestations of Mytilus edulis (L.) by Mytilicola intestinalis Steuer (Copepoda, Cyclopoida). J Cons Int Exp Mer 42:265–271. https://doi.org/10.1093/icesjms/42.3.265
Goater CP, Weber AE (1996) Factors affecting the distribution and abundance of Mytilicola orientalis (Copepoda) in the mussel, Mytilus trossulus, in Barkley Sound, B.C. J Shellfish Res 15:681–684
Goedknegt, MA (2017) Pacific oysters and parasites: Species invasions and their impact on parasite–host interactions. Ph.D. dissertation, Faculty of Earth and Life Sciences, VU University Amsterdam, Amsterdam, The Netherlands
Goedknegt MA, Welsh JE, Drent J, Thieltges DW (2015) Climate change and parasite transmission: how temperature can decrease parasite infectivity via increased predation on infective stages. Ecosphere 6:96. https://doi.org/10.1890/es15-00016.1
Goedknegt MA, Feis ME, Wegner KM, Luttikhuizen PC, Buschbaum C, Camphuysen K, van der Meer J, Thieltges DW (2016) Parasites and marine invasions: ecological and evolutionary perspectives. J Sea Res 113:11–27. https://doi.org/10.1016/j.seares.2015.12.003
Goedknegt MA, Schuster A-K, Buschbaum C, Gergs R, Jung AS, Luttikhuizen PC, van der Meer J, Troost K, Wegner KM, Thieltges DW (2017) Spillover but no spillback of two invasive parasitic copepods from invasive Pacific oysters (Crassostrea gigas) to native bivalve hosts. Biol Invasions 19:365–379. https://doi.org/10.1007/s10530-016-1285-0
Goedknegt MA, Bedolfe S, Drent J, van der Meer J, Thieltges DW (2018a) Impact of the invasive parasitic copepod Mytilicola orientalis on native blue mussels Mytilus edulis in the western European Wadden Sea. Mar Biol Res 14:497–507. https://doi.org/10.1080/17451000.2018.1442579
Goedknegt MA, Thieltges DW, van der Meer J, Wegner KM, Luttikhuizen PC (2018b) Cryptic invasion of a parasitic copepod: compromised identification when morphologically similar invaders co-occur in invaded ecosystems. PLoS One 13:e0193354. https://doi.org/10.1371/journal.pone.0193354
Goedknegt MA, Nauta R, Markovic M, Buschbaum C, Folmer EO, Luttikhuizen, van der Meer J, Waser AM, Wegner KM, Thieltges DW (2019) How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale. Royal Netherlands Institute for Sea Research (NIOZ) Dataset. https://doi.org/10.4121/uuid:5cbdda90-ebfe-4fd9-a82d-89c9e0b2b519
Grainger JN (1951) Notes on the biology of the copepod Mytilicola intestinalis Steuer. Parasitology 41:135–142. https://doi.org/10.1017/s0031182000083967
Gräwe U, Flöser G, Gerkema T, Duran-Matute M, Badewien TH, Schulz E, Burchard H (2016) A numerical model for the entire Wadden Sea: skill assessment and analysis of hydrodynamics. J Geophys Res Oceans 121:5231–5251. https://doi.org/10.1002/2016jc011655
Harms J, Anger K (1983) Seasonal, annual and spatial variation in the development of hard bottom communities. Helgolӓnder wiss Meeresunters 36:137–150. https://doi.org/10.1007/bf01983853
Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc R Soc B 272:1059–1066. https://doi.org/10.1098/rspb.2005.3070
Ho J-S, Kim I-H (1992) Copepod parasites of Gastropoda from Korea. Korean J Zool 35:240–255
Hockley AR (1951) On the biology of Mytilicola intestinalis (Steuer). J Mar Biol Assoc UK 30:223–232. https://doi.org/10.1017/s0025315400012728
Jackson MC, Grey J (2013) Accelerating rates of freshwater invasions in the catchment of the River Thames. Biol Invasions 15:945–951. https://doi.org/10.1007/s10530-012-0343-5
Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Biol 213:961–970. https://doi.org/10.1242/jeb.037721
Katkansky SC, Sparks AK, Chew KK (1967) Distribution and effects of the endoparasitic copepod, Mytilicola orientalis on the Pacific oyster, Crassostrea gigas, on the Pacific coast. Proc Nat Shellfish Assoc 57:50–58
Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498. https://doi.org/10.1111/j.1461-0248.2006.00885.x
Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins KM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056. https://doi.org/10.1890/08-1085.1
Kent RML (1979) The influence of heavy infestations of Polydora ciliata on the flesh content of Mytilus edulis. J Mar Biol Assoc UK 59:289–297. https://doi.org/10.1017/s0025315400042594
Kent RML (1981) The effect of Polydora ciliata on the shell strength of Mytilus edulis. J Cons Int Explor Mer 39:252–255. https://doi.org/10.1093/icesjms/39.3.252
Kopp K, Jokela J (2007) Resistant invaders can convey benefits to native species. Oikos 116:295–301. https://doi.org/10.1111/j.0030-1299.2007.15290.x
Korringa P (1968) On the ecology and the distribution of the parasitic copepod Mytilicola intestinalis Steuer. Bijd Dierkunde 38:47–57
Lauckner G (1983) Diseases of mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals. Biologische Anstalt Helgoland, Hamburg, pp 477–1083
Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326. https://doi.org/10.1046/j.1523-1739.2003.02038.x
Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 3:171–177. https://doi.org/10.1016/j.ijppaw.2014.04.002
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.1890/1051-0761(2000)010%5b0689:bicegc%5d2.0.co;2
Mordecai EA (2013) Despite spillover, a shared pathogen promotes native plant persistence in a cheatgrass-invaded grassland. Ecology 94:2744–2753. https://doi.org/10.1890/13-0086.1
Mori T (1935) Mytilicola orientalis, a new species of parasitic Copepoda. Zool Soc Jpn 47:687–693
Mouritsen KN, McKechnie S, Meenken E, Toynbee JL, Poulin R (2003) Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. J Mar Biol Assoc UK 83:307–310. https://doi.org/10.1017/s0025315403007124h
Nikolaev KE, Sukhotin AA, Galaktionov KV (2006) Infection patterns in White Sea blue mussels (Mytilus edulis L.) of different age and size with metacercariae of Himasthla elongata (Echinostomatidae) and Cercaria parvicaudata (Renicolidae). Dis Aquat Organ 71:51–58. https://doi.org/10.3354/dao071051
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 2.5-4
Paterson RA, Townsend CR, Poulin R, Tompkins DM (2011) Introduced brown trout alternative acanthocephalan infections in native fish. J Anim Ecol 80:990–998. https://doi.org/10.1111/j.1365-2656.2011.01834.x
Paterson RA, Lal A, Dale M, Townsend CR, Poulin R, Tompkins DM (2013) Relative competence of native and exotic fish hosts for two generalist native trematodes. Int J Parasitol Parasites Wildl 2:136–143. https://doi.org/10.1016/j.ijppaw.2013.03.004
Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299. https://doi.org/10.1016/s1471-4922(03)00117-x
Pogoda B, Jungblut S, Buck BH, Hagen W (2012) Infestation of oysters and mussels by mytilicolid copepods: differences between natural coastal habitats and two offshore cultivation sites in the German Bight. J Appl Ichtyol 28:756–765. https://doi.org/10.1111/jai.12025
Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode species. Parasitology 132:134–151. https://doi.org/10.1017/s0031182005008693
Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshw Biol 56:676–688. https://doi.org/10.1111/j.1365-2427.2010.02425.x
Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164:79–89. https://doi.org/10.1086/424610
Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390. https://doi.org/10.1016/j.tree.2004.05.002
Reise K (1998) Pacific oysters invade mussel beds in the European Wadden Sea. Mar Biodivers 28:167–175. https://doi.org/10.1007/bf03043147
Reise K, Buschbaum C, Büttger H, Wegner KM (2017) Invading oysters and native mussels: from hostile takeover to compatible bedfellows. Ecosphere 8:e01949. https://doi.org/10.1002/ecs2.1949
Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:634–689. https://doi.org/10.1146/annurev.ecolsys.36.102003.152638
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 13 Dec 2016
Searle CL, Cortez MH, Hunsberger KK, Grippi DC, Oleksy IA, Shaw CL, de la Serna SB, Lash CL, Dhir KL, Duffy MA (2016) Population density, not host competence, drives patterns of disease in an invaded community. Am Nat 188:554–566. https://doi.org/10.1086/688402
Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2014) Generalized linear mixed models using AD model builder. R package version 0.8.0
Steele S, Mulcahy MF (2001) Impact of the copepod Mytilicola orientalis on the Pacific oyster Crassostrea gigas in Ireland. Dis Aquat Organ 47:145–149. https://doi.org/10.3354/dao047145
Steuer A (1902) Mytilicola intestinalis n. gen. n. spec. aus dem Darme von Mytilus galloprovincialis Lam. (Vorläufige Mittheilung). Lam Zool Anz 25:635–637
Stier T, Drent J, Thieltges DW (2015) Trematode infections reduce clearance rates and condition in blue mussels Mytilus edulis. Mar Ecol Prog Ser 529:137–144. https://doi.org/10.3354/meps11250
Stringer AP, Linklater WL (2015) Host density drives macroparasite abundance across populations of a critically endangered megaherbivore. Oecologia 179:201–207. https://doi.org/10.1007/s00442-015-3319-1
Stunkard HW (1964) Studies on the trematode genus Renicola: observations on the life history, specificity and systematic position. Biol Bull 126:468–489. https://doi.org/10.2307/1539314
Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128. https://doi.org/10.1079/joh2006364
Telfer S, Brown K (2012) Invasions and infections—the effects of invasion on parasite dynamics and communities. Funct Ecol 26:1288–1299. https://doi.org/10.1111/j.1365-2435.2012.02049.x
Thieltges DW, Reise K (2007) Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150:63–68. https://doi.org/10.1007/s00442-006-0557-2
Thieltges DW, Rick J (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Dis Aquat Organ 73:63–68. https://doi.org/10.3354/dao073063
Thieltges DW, Krakau M, Andresen H, Fottner S, Reise K (2006) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgol Mar Res 60:307–316. https://doi.org/10.1007/s10152-006-0046-3
Thieltges DW, Bordalo MD, Hernández AC, Prinz K, Jensen KT (2008) Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology 135:1111–1116. https://doi.org/10.1017/s0031182008004526
Thieltges DW, Reise K, Prinz K, Jensen KT (2009) Invaders interfere with parasite–host interactions. Biol Invasions 11:1424–1429. https://doi.org/10.1007/s10530-008-9350-y
Troost K (2010) Causes and effects of a highly successful marine invasion: case-study of the introduced Pacific oyster Crassostrea gigas in continental NW European estuaries. J Sea Res 64:145–165. https://doi.org/10.1016/j.seares.2010.02.004
Vitousek P, D’Antonio C, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Warner GF (1997) Occurrence of epifauna on the periwinkle, Littorina littorea (L.), and interactions with the polychaete Polydora ciliata (Johnston). Hydrobiologia 355:41–47. https://doi.org/10.1023/a:1003011020446
Waser AM (2018) Predation on intertidal mussels: Influence of biotic factors on the survival of epibenthic bivalve beds. Ph.D. dissertation, Faculty of Earth and Life Sciences, VU University Amsterdam, Amsterdam, The Netherlands
Welsh JE, van der Meer J, Brussaard CPD, Thieltges DW (2014) Inventory of organisms interfering with transmission of a marine trematode. J Mar Biol Assoc UK 94:697–702. https://doi.org/10.1017/s0025315414000034
Werding B (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Mar Biol 3:306–333. https://doi.org/10.1007/bf00698861
Wilson JG, Galaktionov KV, Sukhotin AA, Skirnisson K, Nikolaev KE, Ivanov MI, Bustnes JO, Saville DH, Regel KV (2011) Factors influencing trematode parasite burdens in mussels (Mytilus spp.) from the north Atlantic Ocean across to the north Pacific. Estuar Coast Shelf Sci 132:87–93. https://doi.org/10.1016/j.ecss.2011.10.005
Acknowledgements
We are grateful to B.D.H.K. Eriksson of the University of Groningen (The Netherlands) for the provision of lab space during our field sampling campaign. We also thank the volunteers who assisted us with transport, field and lab work: Ewout Adriaans, Christian Einer, Jarco Havermans, Jonas Martin, Fokje Schaafsma, and Samira Theis. For the permission to use bird data from the Trilateral Monitoring and Assessment Programme (TMAP) carried out in the Wadden Sea by The Netherlands, Germany and Denmark, we thank SOVON (in particular Erik van Winden), Rijkswaterstaat, Wageningen Marine Research (WMR), Staatliche Vogelschutzwarte (Lower Saxony Water Management, Coastal Defence and Nature Conservation Agency NLWKN), National Park Authority for the Wadden Sea Lower Saxony Norbert Kempf, Schleswig–Holstein Agency for Coastal Defence, National Park and Marine Conservation-National Park Authority (LKN SH), Danish Centre for Environment and Energy (DCE) and Aarhus University. This study was financially supported by the Netherlands Organization for Scientific Research (NWO) and the German Bundesministerium für Bildung und Forschung (BMBF) (NWO-ZKO Project 839.11.002).
Author information
Authors and Affiliations
Contributions
MAG, DWT and JVDM conceived and designed the study. MAG, RN, MM, CB and KMW conducted fieldwork. MAG, RN and MM performed parasite dissections. PCL conducted the molecular identification. EOF and AMW compiled data on biotic and environmental variables. MAG conducted the statistical analyses with input from JVDM. MAG and DWT wrote the manuscript with significant contributions of all other authors.
Corresponding author
Additional information
Communicated by Peter S. Petraitis.
M. Anouk Goedknegt: currently working in the Universite de Bordeaux, UMR 5805 EPOC, Station Marine d’Arcachon, 2, Rue du Professeur Jolyet, 33120 Arcachon, France.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Goedknegt, M.A., Nauta, R., Markovic, M. et al. How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale. Oecologia 190, 99–113 (2019). https://doi.org/10.1007/s00442-019-04408-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04408-x