title for learn-about section of A SNAIL'S ODYSSEY
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Settlement, metamorphosis, & recruitment


The topic of settlement & metamorphosis is considered here, while SPAWNING & LARVAL LIFE can be found elsewhere.

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Research study 1

photograph of juvenile mussel Mytilus californianus attached to seaweedAt the end of their pelagic life, the larvae of mussels are attracted to settle in the proximity of adults.  However, owing to the risk of adults sucking them in, or perhaps to avoid competition with adults at too small a size, the larvae seek out and attach to “secondary” substrates – usually nearby seaweeds.  Only later, at a larger, more competitively advantageous size, do they crawl down onto the primary rock substrate and adopt the adult way of life. Later, at a size of about 1mm, the juveniles may release their attachments to the seaweeds and be transported by water currents in a secondary migration to new habitats.  Enabling this is the secretion of a long byssus thread that, like the gossamer threads of baby spiders, carries the youngsters along in relatively small currents through force of viscous drag.  Bayne 1964 J Anim Ecol 33: 513; Sigurdsson et al. 1976 Nature 262: 386.

NOTE  designates substrates other than the “primary” rock surface to which most of the juveniles will eventually attach when they grow larger.  This is often referred to as primary and secondary settlement behaviour by mussel larvae

NOTE  byssus threads are described in detail in another part of this LEARN-ABOUT section on mussels: ANCHORING

Juvenile mussel Mytilus trossulus
attaches to a seaweed Fucus sp. 1X


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Research study 2

histogram showing settlement of larval mussels on different substrataData on settlement of mussels near San Diego, California show that Mytilus galloprovincialis avoids its superior competitor M. californianus when settling, but also that larval M. californianus avoid adults of M. galloprovincialis.  The main difference between this study and one done in Oregon (see Research Study 3 below) is that settlement by larvae of M. californianus appears less random and, as mentioned, includes strong avoidance of the other species.  Another feature of interest is that settling M. galloprovincialis tend to attach to juvenile conspecifics, whereas juvenile M. californianus tend to attach to adult conspecifics. Petraitis 1978 Veliger 21: 288.

NOTE  the author uses plastic ice-cube trays with the different substrata enclosed within.  These are placed in different parts of the shore and left for 3.5mo.  At the end of the experiment, the number of settled spat of each mussel species on each substratum is counted. Seaweeds are not included in the selection of substrata in the ice-cube trays 

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Research study 3

Lab studies in Oregon on comparative settling preferences of larval mussels present a slightly different picture. Thus, larvae of bay mussels Mytilus trossulus preferentially settle on filamentous algae and adults of their own species, but avoid sea mussels M. californianus.  However, larvae of M. californianus settle broadly and show little or no avoidance of M. trossulus.  Thus, 2 contrasting settlement strategies have evolved, one where an inferior species M. trossulus avoids areas where competition is intense and chances of survival are low; the other, where a competitively dominant species undergoes little selection pressure to avoid specific habitats.  Petersen 1984 J Exp Mar Biol Ecol 82: 147.

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Research study 4

photograph of a mussel Mytilus trossulus attached to surf grass Phyllospadix scouleriField distributions of juveniles, 1-10mm shell length, of Mytilus californianus in Oregon support the notion put forward in the preceding Research Study.  Their presence on many different types of substrata including their own adults, adults of M. trossulus, bare rock, and filamentous algae, especially the red alga Endocladia muricata, helps explain the dominance and broad geographic range of the species.  Therefor, unlike in other species of mussels, such as M. trossulus and M. galloprovincialis, there appears to be little or no secondary settlement of small juveniles of M. californianusPetersen 1984 Veliger 27: 7.




Juvenile mussel Mytilus trossulus attached to
a blade of eelgrass Phyllospadix scouleri 1X

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Research study 5

graph showing growth rates of mussel Mytilus californianus larvae on different rations of phytoplankton foodgraph showing lipid contents of 2-wk larvae of mussels Mytilus californianus raised on different concentrations of phytoplankton foodThere has been much research attention on “condition1” of marine-invertebrate larvae and how variation in condition, even within a single cohort of larvae, may affect recruitment success.  Research in southern California on Mytilus galloprovincialis indicates that larvae raised in the laboratory under high food concentrations2 are larger at metamorphosis (see graph upper Left) and have significantly higher lipid levels than ones raised under lower food concentrations (see graph on Right).

histogram showing effect of
So far there is nothing particularly novel in these findings, but now the researcher does something interesting.  Half of the newly metamorphosed juveniles from these larval cultures are outplanted in the field3 for 2wk, both intertidally and subtidally, and the other half are reared in the laboratory at 2 different juvenile rations for a further 20d.  In all cases, juveniles raised with high larval rations display higher growth rates and attain larger sizes than those raised on lower food rations (see graph lower Left). Interestingly, for the field mussels there is no effect of tidal position on growth over 2wk following metamorphosis.  Thus, individuals growing intertidally do just as well as ones growing subtidally. Overall, field conditions are more favourable for juvenile growth than laboratory conditions (data not shown here).  In all cases, mortality is lower for juveniles raised on high larval rations than for ones raised on low larval rations, suggesting that vulnerability to early juvenile mortality may also be affected by larval history.  Why do individuals that eat better as larvae do better as juveniles? Likely because the extra lipid reserves simply give them a “head-start”. Phillips 2002 Ecology 83: 2562.

NOTE1  defined here as content of lipid in the larva

NOTE2  3 concentrations of 1:1 mix of Dunaliella tertiolecta and Isochrysis galbana are used: 20 000, 2000, and 500 cells . ml-1

NOTE3  the mussels are metamorphosed onto plastic scrub pads glued to bits of plastic and suspended from a pier on cables, at depths corresponding to subtidal and intertidal habitats.  The mussels are marked with calcein (a fluorescent dye, concentration of 0.15g . ml-1) to distinguish them later from any “wild” settlers

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Research study 6

map of collection sites for settlement/recruitment study on mussels Mytilus spp. in Californiahistogram showing size of mussel recruits at sites north and south of Point Conceptionhistogram showing seasonal variation in settlement/recruitment of mussels at sites around Point Conception, CaliforniaResearchers at the Marine Science Institute, UC Santa Barbara address the question of whether mussel recruits differ in size at intertidal sites on either side of Point Conception, California (see map).  The expectation, given that phytoplankton food resources are more plentiful in the rich upwelling zone north of the Point, would be that recruits in the north would be larger than those in the south.  Indeed, results show that larvae settling at the most southern site in Santa Barbara Channel are significantly smaller than those settling at 3 of the 4 most northern sites (see histogram above Right).  Additionally, early-season settlers are significantly larger than mid-season or late-season ones, likely reflecting greater availability of food for the veligers in springtime (see histogram lower Right).  Variability in the data is high, and some interactions, most notably site and season, are not significant.   Phillips & Gaines 2002 Invert Repr Dev 41: 171.

NOTE  molecular-genetics analyses show that mussels settling are likely to have been a mix of about 80% Mytilus californianus and 20% M. galloprovincialis.  Recruits are defined as being <1mo post-settlement

NOTE  plastic scrubbing pads (Tuffy brand) are attached at mid-intertidal locations at each of the 6 study sites and monitored monthly for settlers 

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Research study 7

map of Sunset Bay, Oregon showing foam lineThe importance of upwelling and downwelling events on settlement of mussel larvae is emphasised in a study by researchers at the Oregon Institute of Marine Biology, Charleston.  The authors notice a ribbon of foam along the entrance to Sunset Bay and hypothesise that conditions creating it may be blocking shoreward movement and subsequent settlement of larvae within the Bay.  Indeed, collection of physical and biological oceanographic data combined with information from settlement trays moored at 3 locations within and without the Bay (see map) confirm that during downwelling winds the front is stable and consists of a wall of cooler, saltier and denser offshore water separated from that within the Bay.  During such times mussel veligers are more concentrated seaward of the front;  during downwelling winds, the front breaks down and the larvae are more evenly distributed.  McCulloch & Shanks 2003 J Plankton Res 25 (11): 1427.

NOTE  the study deals both with mussel and barnacle settlement, but only the former is considered here

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Research study 8

map showing larval release and juvenile collecting sites in a study of mussel "connectivity"histograms showing "connectivity" of mussels populations in southern CaliforniaChemical “fingerprinting2” of larvae is becoming increasingly popular as a way to determine connectivity of populations.  Recently, researchers at Scripps Institution of Oceanography, California use the technique to compare distribution of larvae of mussels Mytilus californianus and M. galloprovincialis, and they show that despite similar larval morphologies and behaviour, the connectivity patterns of the 2 species are quite different.  The researchers culture larvae of both species in situ at 13 sites over 75km of coastline and monitor larval distributions by collecting new recruits and matching their chemistries2 with those at the original culture sites (see map). To discriminate between new recruits of the 2 species, which are difficult to tell apart visually, the researchers use a molecular-genetic assay, which works about 40% of the time.  However, by combining this technique with shell chemistry and certain morphological features of the shell, the accuracy of the identification increases to greater than 85%. Results show, firstly, that distributional distances of the larvae are much less than anticipated, often no more than 20-30km from their origins.  Secondly, the predictive ability of the method seems good, as illustrated in the histograms3 on the Right.  Greater connectivity is indicated by the degree of homogeneity in bar colour. Note that the connectivity levels of the M. californianus sites is much greater than than that of the M. galloprovincialis sites.  Generally, most larval transport is from north to south, with the M. galloprovincialis recruits exhibiting more diverse origins (northern: 45%, southern: 47%, and San DiegoBay: 7%).  In comparison, most M. californianus recruits originate from the northern part of the study area.  The reasons for these differences in 2 otherwise similar species are not known.  Becker et al. 2007 Proc Nat Acad Sci 104 (9): 3271; for further information from the same research group on the feasibility of using elemental-fingerprinting methods on mussels see Becker et al. 2005 Limnol Oceanogr 50 (1): 48, Fodrie et al. 2011 J Sea Res 65: 141, and Carson et al. 2013 Mar Ecol Progr Ser 473: 133.

NOTE1  the method identifies the pattern of elements incorporated into the larval shells before they hatch, then matches this pattern with the microchemistry of the larval structures retained after settlement and metamorphosis, thus enabling the location where the hard part was formed to be identified.  For information on the application of the method to crab larvae see Research Studies 2 & 3 in LEARNABOUT CRABS & RELATIVES: SETTLEMENT,  METAMORPHOSIS, & RECRUITMENT: OTHER DECAPOD SPECIES

NOTE2   the isotopes monitored are those of Ca, Mn, Co, Sr, Ba, Pb, U, and Sn

NOTE3  collection sites of the juveniles are shown on the X axis, while the natal-origin sites are shown by the coloured components of each bar.  Blue colours represent the more northern sites, and red/orange colours the more southern sites.  Sites in San Diego Bay are shown in green.  Twelve of the release locations are duplicated, so the total number of natal sites is 25 (see vertical row of coloured squares on the Right) 

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Research study 9

histogram showing settlement of mussel larvae Mytilus spp. at 3 locations near Moss Landing, CaliforniaTo what extent are adult distributions explained by preferential larval settlement, versus differential post-settlement survival?  This age-old question is addressed for mussels Mytilus californianus, M. galloprovincialis, and M. trossulus at sites near Moss Landing, California.  The researchers compare settlement and recruitment of the 3 species, at roughly 2wk intervals for a year, on fibrous scrubbing pads set out in 3 locations: a wave-exposed jetty, within the protected harbor, and in the channel between them.  Results show greatest settlement of all species on the jetty, where adult M. californianus are most common, than in the harbor where adult bay mussels M. galloprovincialis and M. trossulus are most common (see histogram).  Almost all larval M. californianus settle on the jetty where their adults are most common. and few to none settle in the bay. In contrast, the 2 bay-mussel species settle abundantly on the jetty, and also in the other 2 locations. Maximum settlement of all species occurs in pulses during the year, in May, August, and November. Thus, the 2 bay-mussel species settle widely, while the California mussel is more site-specific.  The fact that bay mussels settle abundantly on the jetty, but then die, suggests that post-settlement mortality is likely the most important influence on distribution of the adults.  Johnson & Geller 2006 J Exp Mar Biol Ecol 328: 136.  

NOTE  the species are identified through genetic markers: taxon-specific polymerase chain-reactions.  The researchers are able to distinguish all 3 larval types both from planktonic collections and from collections on the shore

NOTE  the degree of wave exposure at the sites is jetty>channel>harbor

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Research study 10

map showing study sites for mussel-recruitment researchPoint Conception, California has long been known as an important biogeographic discontinuity on the west coast.  High wave-exposure and strong upwelling of cold, deeper water dominate the coast north of the Point, while weak upwelling and warmer water temperatures dominate the area south of the Point.  Are recruitment and distribution of sea mussels Mytilus californianus affected by these markedly differing conditions?  These questions are addressed in a survey conducted by scientists from the Marine Science Institute, Santa Barbara at a number of sites on either side of the Point (see map) spanning a distance of 300km.  Results show a histograms showing percenatage cover of macrophytes and mussels at locations north and south of Point Conception, Californiadisjunction in community structure, with macroalgae being abundant and mussels being scarce north of the Point, but with mussels being abundant south of the Point (see histograms).  Moreover, mussels are larger south of the Point, and their beds are more expansive and extend lower in intertidal elevation south of the Point (see histogram Fig5 just use %cover).  A histograms showing percentage cover of mussels at sites north and south of Point Conception, Californiagreater abundance of sea-star predators Pisaster ochraceus and greater wave exposure effectively elevate the upper levels of mussel distribution north of the Point, while south of the Point the beds are displaced to a lower level.  Contrary to what they expected, the researchers could find no significant difference in mussel recruitment on either side of the Point to explain the difference in spatial distributions.  Blanchette & Gaines 2007 J Exp Mar Biol Ecol 340: 268.

NOTE  seawater temperatures are about 4oC warmer south of the Point

NOTE  recruitment rates measured using plastic mesh-ball collectors of “Tuffys”.  Mussel recruits are not separated by species, but 90% or more are cofirmed by genetic examination to be M. californianus

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Research study 11

drawing of moored assembly for monitoring mussel-larvae abundance offshoreIt seems logical that the greater the abundance of competent larvae in nearshore waters, the greater will be the rate of intertidal recruitment, but is this true?  In fact, a several-year study by researchers at Oregon State University using data obtained from collectors mounted at different depths on moorings anchored 50-1100m from shore, and from collectors on the shore, show that while abundances of competent larvae of mussels Mytilus californianus and M. trossulus in nearshore areas remains relatively uniform from year to year, onshore recruitment varies considerably and is unrelated to larval abundance.  Other data indicate that nearshore larval distribution is stratified vertically, and this may have an effect on the extent of transport through the surf zone and ultimate recruitment.  The authors conclude that the key to understanding how larvae are transported shoreward lies within the surf zone itself, an area they term a “semi-permeable barrier”. Yet, processes occurring in the surf zone are still poorly understood.  The study provides an enormous body of information of pelagic-benthic coupling, and the short account presented here does not do it justice.  Rilov et al. 2008 J Exp Mar Biol Ecol 361: 59.

NOTE  a parallel study in New Zealand yields similar results, not considered here

NOTE  these are plastic-mesh pot-scrubbers or “Tuffies” used by the same researchers in other similar studies.  They are suspended on lines moored to the sea bottom, along with larval traps, current meters, and temperature recorders (see accompanying illustration).  Replicate sites are monitored during summer periods over different years in Oregon at Cape Foulweather and Cape Perpetua, and at 2 other locations

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Research study 12

Predictions on how climate change will modify marine ecosystems are often made difficult by lack of long-term data sets.  However, in an investigation on potential effects on recruitment of sea mussels Mytilus californianus, researchers at Oregon State University, Corvallis are able to use 14-18yr data sets relating phytoplankton abundance with recruitment at 10 locations along 320km of Oregon coastline.  Results show, as expected, that phytoplankton abundance and mussel recruitment are positively correlated. In general, strongest correlations of phytoplankton abundance/recruitment are with North Pacific Gyre Oscillation-type current patterns (7-10yr durations), and weaker with other types.  The authors conclude that mussel recruitment and other processes will continue to be sensitive to future long-term climatic fluctuation.  However, they further note that, despite such effects in the past, mussel population dynamics and other community dynamics have changed little, and suggest that local ecological interactions may act to dampen effects of impending climate change.   Menge et al. 2009 Ecol Monogr 79: 379.

NOTE  data for phytoplankton abundance extends over 14yr and for mussel recruitment over 18yr.  Additional input in the analyses include current patterns, tide heights, and sea levels

NOTE  these are El Niño-Southern Oscillation (3-7yr durations) and Pacific Decadal Oscillation (+20yr duration)

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Research study 13

map of southern California showing collecting sites for population-connectivity studydiagram showing population connectivites for mussels Mytilus californianus in November in southern CaliforniaIn Southern California the 2 mussel species Mytilus californianus and M. galloprovincialis have overlapping but different specific adult distributions (open coast and bay, respectively), and different life histories and reproductive timings.  Through a 6yr programme of trace-elemental fingerprinting of larval shells, similar in detail to the methodology employed in Research Study 8 above, researchers at the Scripps Institution of Oceanography, La Jolla document seasonal and year-to-year larval exchange along the coast and within and between embayments.  On the basis of their shell chemistry, 3 source regions for M. californianus are determined: northern, central, and southern, with a 77% assignment accuracy among them (see map). Similarly, 4 source regions are determined for M. galloprovincialis: north coast, central/south coast, Mission Bay, and San Diego Bay, with a 70% assignment accuracy. The extent of movement during larval dispersal of each recruit collected is inferred from its assignment to one of these source regions.  Results show a poleward movement of larvae for both species in autumn (see diagram, data presented only for autumn movement of M. californianus, 3:1 ratio of poleward:equatorward movement), and equatorward movement in springtime, both movements coincidental with direction of near-shore surface currents.  Note in the diagram that self-recruitment to each region is relatively small for M. californianus in November, averaging only about 9% of the total larvae.  In comparison, values for self-recruitment of M. galloprovincialis to the 2 coastal regions average about 16% during the same month.  Overall, through both seasons, open coast-inhabiting M. californianus self-recruit only 28%, significantly less than the 42% self-recruitment of its bay-inhabiting counterpart.  The mean dispersal distances for both species averages about 30km.   Given the marked seasonal variation in connectivity of these mussel populations relating primarily to seasonal changes in water-circulation patterns, the authors underscore the need for similar long-term studies when planning for new Marine Protected Areas, with attention being paid to the possibility of creating ones with flexible boundaries.   Carson et al. 2010 Current Biol 20: 1926; for more on this subject see Carson et al. 2011 Ecology 92 (10): 1972.

NOTE  the researchers culture each species in the laboratory, then “outplant” the embryos twice-yearly to special “larval homes” at several adult sites in San Diego County (overall, 8 such outplantings are done).  After retrieval and chemical analysis via laser-ablation plasma-mass spectroscopy of these larvae, trace-elemental “fingerprints” are created for each larval-source population.  Later collections of newly recruited juveniles and analysis of elemental chemistry of the portions of their shells formed during their early larval dispersals enable the researchers to develop “connectivity maps” for the 6yr study period for both species

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Research study 14

As described in Research Study 1 above, juvenile mussels of several species may employ thread-drifting as a means of secondary or post-settlement dispersal.  Until recently, however, the extent of the behaviour and the hydrographic conditions favouring it have been poorly understood.  To redress this, researchers from the Oregon Institute of Marine Biology, Charleston sample plankton at 4 stations located 0.5-28km from shore 4 times during summer, twice during upwelling conditions, and twice during downwelling (relaxation) conditions, and relate the frequency of occurrence of drifters to oceanographic conditions of wave energy, and winds and surface currents.  Mean sizes of drifters are similar for the species involved (Mytilus californianus and M. trossulus/galloprovincialis), ranging from 350µm to less than 1mm.  Thread lengths are not known because the mucus comprising them fragments during net collection.  Both larval and thread-drifting juveniles are mostly absent in surface waters and at distances greater than 4.5km offshore.  Drifting is common during the months tested (July-August) and local abundances may sometimes be great (>1000 . m-3). Numbers and sizes of drifters are significantly greater during downwelling than upwelling events, but the reasons for this are not clear.  The authors note an absence of correlation with wave energy or alongshore current velocities, but do identify positive correlations of both numbers and sizes of drifters with cross-shelf surface-curent velocities. Shanks & Shearman 2011 Mar Ecol Progr Ser 427: 105.

NOTE  these species are difficult to separate as larvae and juveniles, and so the authors have lumped them.  Based on geography, however, most of these are likely to have been the more northerly occurring species, M. trossulus

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