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Restoring mussel bed: A guide on how to survive on an intertidal mudflat
de Paoli, H.C. (2017). Restoring mussel bed: A guide on how to survive on an intertidal mudflat. PhD Thesis. Rijksuniversiteit Groningen: Groningen. ISBN 978-90-367-9583-8. 172 pp.

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  • de Paoli, H.C., meer

    Restoring mussel bedde Paoli, HeleneIMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish tocite from it. Please check the document version below.Document VersionPublisher's PDF, also known as Version of recordPublication date:2017Link to publication in University of Groningen/UMCG research databaseCitation for published version (APA):de Paoli, H. C. (2017). Restoring mussel bed: A guide on how to survive on an intertidal mudflat[Groningen]: University of GroningenCopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Downloaded from the University of Groningen/UMCG research database (Pure): For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.Download date: 13-02-2017Summary140English SummaryMany coastal ecosystems worldwide have become severely degradedbecause of loss of habitat-modifying ecosystem engineers including saltmarshes, seagrass meadows, mangroves, and coral and shellfish reefs,resulting in a concomitant loss of ecosystem functioning and services.Reef-building shellfish such as mussels and oysters are particularlyimportant on intertidal flats, where they facilitate many species by creatingcomplex and solid structures in an otherwise sandy environment. Yet,similar to many other coastal ecosystems, both oyster and mussel reefshave severely declined over the last decades. In the Wadden Sea, musselbeds covered about 4100 ha of the intertidal mudflats in the 1970s, butaround 1990 this area was reduced to a near 100 ha due to overfishingcombined with natural causes. At present, mussels have only partlyrecovered.In this thesis, I have investigated the mechanisms underlyingpersistence of natural intertidal mussel beds in the Wadden Sea and theprocesses that limit restoration attempts of this important habitat. First, Ihave investigated the importance of the spatial organization of mussel bedsfor their resilience. On natural mussel beds, mussels form complex, nestedpatterns consisting of small 5 to 10-cm strings that in turn make up larger 3to 5-m bands, a pattern that results from the interplay of facilitationbetween the mussels, competition for food, and aggregation into smallclumps. Underneath the large banded aggregations of mussels, faeces andpseudofaeces accumulate, leading to elevated hummocks of organicmatter-rich silt with mussels on top. The effects of mussels bedorganization and of the development of hummocks on the persistence ofmussel beds were studied in two separate experiments, on which I reportin chapter 2 and 3. Second, I have tested whether transplantation ofmussels from subtidal into the intertidal areas could be a feasible approachto restore intertidal mussel beds in the Wadden Sea, on which I report inchapter 4. Finally, I studied in chapter 5 the morphological and behavioral152141differences between subtidal and intertidal mussels in order to understanddifficulty that we encountered in restoring intertidal mussel beds usingsubtidal mussels.Mechanisms underlying mussel bed resilience.To understand how aggregation by mussels at the two spatial scalesaffected their persistence on the intertidal mudflat, I tested how small- andlarge-scale aggregation affected mussel cover over time (Chapter 2) in afully factorial mussel transplantation experiment where we designedartificial mussel beds to have no, any or all types of patterns. Thisexperiment showed that any form of aggregation greatly improved musselbed persistence. Clump formation appeared crucial for perseverance, andaggregation in banded patterns facilitated clump formation; the musselsthen formed clumps themselves. Without any form of aggregation, thedensity of mussels is too low, and they have difficulty moving when aloneon sand. As a consequence, they cannot form the clumps that are essentialto maintain themselves in the habitat. Large-scale bands increase the localdensity to a level that allows mussels to latch on to each other to formclumps that are essential for mussels to survive in this dynamicenvironment.An important consequence of the mussels aggregating in bandedpatches is the formation of hummocks. In chapter 3, I observed that thisincreases water across the top of the hummock in middle of the musselbands. In existing mussel beds, where dislodgment is minimal because themussels are attached to each other by byssus threads, mussel conditionand density was highest on top of the hummocks, most likely because foodavailability increases under the enhanced water flow. In contrast, musselsthat were experimentally transplanted on top of artificial hummocks hadmuch lower survival compared to mussels on flat controls, because thetransplanted mussels were not able to attach sufficiently fast and weredislodged. The effects of hummocks for the mussels appeared a two-edge153142knife, where the positive effects of mussel dominated on the hummocks,but the negative effect dominated in the transplantation experiment,severely reducing survival.Restoration of mussel beds using subtidal musselsEven after understanding the mechanisms and importance of selforganizationfor the persistence of mussel beds, their restoration remaineda significant challenge. In chapter 4, I conducted, in an extensivecollaborative effort, an experimental transplantation of subtidal mussels,creating 36 25x25-m plots on the islands of Terschelling, Ameland andSchiermonnikoog. According to the principles outlined above, the bedswere built on a flat substrate with a density that allowed mussels to formclumps. In addition, the potential importance of sediment stabilizingsubstrate was tested by adding coconut fiber net to half of the plots. I thenfollowed the persistence of these artificial mussel beds for a number ofmonths, expecting them to survive at least for a few years. Surprisingly,however, all the beds disappeared between 3 (on Ameland) and 7 months(on Terschelling) time. Neither predation by birds and crabs, nordisturbance by waves stress could not explain differences in survivalbetween islands. However, the fact that the beds started to disappear fromthe edge strongly suggest that waves are the most important factor drivingthe rapid disappearance of the experimental mussel beds.Next, I investigated whether the fast collapse of the transplantedbeds was due to the use of mussels from subtidal areas, hypothesizing thatthese mussels could not adapt to their new intertidal environment(Chapter 5). To this end, I first compared the survival of sub- and intertidalmussels in a smaller field experiment near Schiermonnikoog. Thecomparison revealed that intertidal mussels were much better adapted tothe intertidal habitat then subtidal mussels; after 20 days, 70% of allintertidal mussels survived, while only 2% of subtidal mussels survived.Furthermore, a comparison of morphological characteristics revealed that154143the shells of subtidal mussels were 3 times lighter than those of intertidalmussels, making subtidal mussels more vulnerable to predation by birdsand crabs. Finally, laboratory experiments demonstrated that attachmentto substrate by intertidal mussels was 3 times higher compared to subtidalmussels, making the latter more vulnerable to hydrodynamic stress as well.From the comparison of the intertidal and the subtidal mussels, Iconclude that subtidal mussels were not well adapted to the intertidalenvironment to which they were exposed in the transplantationexperiments. I then investigated whether these striking difference could beexplained by genetic differences between sub- and intertidal mussels.However, genetic analysis showed that despite their differences inmorphology and behavior, subtidal and intertidal mussels did not appearto differ much genetically, suggesting that phenotypic adaptation as a likelydriving mechanism for the observed differences. This highlights an issuethat is of broad relevance to restoration science: is it always possible torestore a specific habitat or species by transplanting organisms from otherareas, or can maladaptation of the transplanted organisms then limitrestoration success?ConclusionMy thesis highlighted that mussel do shape their own environmentenhancing their survival and access to resources. This finding hasimportant implications for future restoration projects. At first sight, musseltransplantation may appear a good restoration technique, as it would allowmussels to quickly (re) built their environment. However, mussel do notonly shape their own environment, but their environment also shapesthem. Intertidal mussels have a morphology and a behavior that allowthem to survive in a dynamic area. Subtidal mussels are not adapted tointertidal conditions and cannot survive on an intertidal mudflat, makingtransplantation not suitable to restore intertidal beds. A possible technique155144to restore mussel beds would consist in simulating natural mussel bedconditions to increase recruitment.

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