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Comparison of phototrophic shell-degrading endoliths in invasive and native populations of the intertidal mussel Mytilus galloprovincialis

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Abstract

The intertidal mussel Mytilus galloprovincialis is a successful invader worldwide. Since its accidental introduction onto the South African west coast in the late 1970s, it has become the most successful marine invasive species in South Africa. One possible explanation for this phenomenon is that M. galloprovincialis suffers less from phototrophic shell-degrading endoliths in its invasive than in its native range. We assessed photoautotrophic endolithic pressure on M. galloprovincialis in native (Portugal) and invasive (South Africa) ranges. Invasive populations were more heavily infested than native populations. In Portugal, only the biggest/oldest mussels displayed endolithic erosion of the shell and the incidence of infestation was greater at higher shore levels where more prolonged exposure to light enhances endolith photosynthesis. In South Africa, even the smallest size classes of mussels were heavily infested throughout the shore. In Portugal, endolithic-induced mortality was observed at only one location, while in South Africa it occurred at all locations and at significantly higher rates than in Portugal. Important sub-lethal effects were detected in infested native mussels, confirming previous studies of invasive populations and suggesting an energy trade-off between shell repair and other physiological constraints. We observed a positive relationship between infestation rates and barnacle colonization on mussel shells, suggesting possible facilitation of barnacle settlement/survival by shell-boring pathogens. Identification of endoliths revealed common species between regions. However, two species were unique in the invasive range while another was unique in the native region. Different levels of endolithic infestation in the invasive and the native range were not explained by the effect of major environmental determinants (Photosynthetically Available Radiation and wave height). The results reject our initial hypothesis, indicating that invasion success of M. galloprovincialis is not simply explained by escape from its natural enemies but results from complex interactions between characteristics of the invaded community and properties of the invader.

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Acknowledgments

This research was supported by post-doctoral fellowships from FCT, Portugal (to GIZ) and funded by project PTDC/BIA-BEC/103916/2008 from FCT (to GIZ). The authors thank C. Florindo (Universidade do Algarve, Cell Imaging Unit; Dept. de Ciencias Biomédicas e Medicina) for her help with preparing samples and microscopy image analysis, and A. Morgado-André and F. Oliveira (Universidade do Algarve, Civil Engineering Department, Escola Superior de Tecnologia) for their assistance in the use of the compression equipment. This work is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation. We thank also two anonymous referees for helpful comments.

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  1. CCMAR-CIMAR Laboratorio Associado, Universidade do Algarve, Faro, Portugal

    Nathalie Marquet, Katy R. Nicastro, Gareth A. Pearson, Ester A. Serrão & Gerardo I. Zardi

  2. Institute of Paleontology, Friedrich Alexander University, Erlangen, Germany

    Marcos Gektidis

  3. Department of Zoology and Entomology, Rhodes University, Grahamstown, 6140, South Africa

    Christopher D. McQuaid

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  1. Nathalie Marquet
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Correspondence to Nathalie Marquet.

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10530_2012_363_MOESM2_ESM.pptx

Figure 1S. Examples of shells at varying stages of endolith infestation. Shells with clean, intact periostracum and distinct outer growth lines (Group A); shells with central portion of surface eroding and turning pale purple, outer growth lines becoming indistinct (Group B); shells with erosion spreading past central portion, grooves and pits appearing on shell surface (Group C); shells heavily pitted and becoming deformed, outer growth lines almost completely absent (Group D); shells extremely pitted, deformed and brittle, eventually holed (Group E). Scale bar = 1cm. (PPTX 114 kb)

10530_2012_363_MOESM3_ESM.tif

Figure 2S. Microbial endoliths of M. galloprovincialis. Euendoliths depicted in this plate from A to D exhibit a specific habitus, which allows a taxonomic classification to genus level. Euendoliths depicted from E to F were not found in sufficient numbers or did not exhibit typical habitus for a definite taxonomic identification. (A - D) Euendoliths of cyanobacterial origin and members of the genus Hyella. In (A) arrow points to an elongated terminal cell. Filaments are long and cells arranged in a single row. Terminal cell always much longer than subterminal cell. In (B) arrow points to a large cluster of baeocytes, which gives the colony an arachnoid appearance. (E - F) Unidentified euendoliths of cyanobacterial origin. Habitus and cell size place this species close to the genus Solentia. The red colour is maintained next to green coloured cells of another species. This and the large cell size place this species very close to Solentia sanguina. However, neither the very prominent layered sheath, nor the frequent ramification of S. sanguina were observed in this colony. In (E) arrow points to a terminal cell. In (F) arrow points to the enhanced distance between terminal and subterminal cell. (TIFF 11988 kb)

10530_2012_363_MOESM4_ESM.tif

Figure 3S. Microbial endoliths of M. galloprovincialis. Euendoliths depicted in this plate were not found in sufficient numbers or did not exhibit typical habitus for a definite taxonomic identification. (A) Heterotrophic endolith, presumably of fungal origin. Arrow points to tunnel entrance. (B) Euendolith of cyanobacterial origin. Habitus and cell size place this organism close to the genus Hyella or Solentia. Arrow points to barely visible gelatinous sheath. Terminal cells are elongated and at a greater distance to subterminal cells, which is characteristic of Solentia. (C) Euendolith of cyanobacterial origin. Habitus and cell size place this species close to Hyella or Cyanosaccus. Hyella is more likely, because at some points, the cell number exceeds four. Baeocytes are packed as in Hyella immanis or H. conferta. Arrow shows retouched area, where the original scale had been burned into the picture and then manually removed from the picture. (D) Euendolith of cyanobacterial origin. Habitus and cell size place this species close to Hyella or Solentia. Pink colour might be an artifact or pigmentation like with Solentia sanguina but this species is much smaller than S. sanguina (CL ~24µm CW~14 µm). Arrow points to elongated terminal cell. (E) Euendolith of cyanobacterial origin. Habitus and cell size place this species close to Hyella. Baeocytes are packed as in Hyella immanis or H. conferta. (F) Euendolith of cyanobacterial origin. Habitus and cell size place this species close to Hyella. Arrow points to vegetative cells surrounded by sheath. (TIFF 10709 kb)

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Marquet, N., Nicastro, K.R., Gektidis, M. et al. Comparison of phototrophic shell-degrading endoliths in invasive and native populations of the intertidal mussel Mytilus galloprovincialis . Biol Invasions 15, 1253–1272 (2013). https://doi.org/10.1007/s10530-012-0363-1

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  • DOI: https://doi.org/10.1007/s10530-012-0363-1

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