Attachrnent strength and reproductive condition

Attachrnent strength and reproductive condition

BIOTIC AND ABIOTIC INFLUENCES ON THE ATTACHMENT STRENGTH OF BLUE MUSSEL (MYTILUS EDULIS) FROM SUSPENDED CUL TURE, IN THE MAGDALEN ISLANDS (QUEBEC, CANADA) :

Mussel growers take advantage of a characteristic behavior of mussels, namely their capacity of self-attachment to substratum, to get a simplified culture system avoiding containment in cages, trays, etc. In Atlantic Canada, mussels are mostly produced in suspended culture on submersible longlines to provide against the ice coyer (Mallet and Carver 1991, Mallet and Myrand 1995). Soon after sleeving, the young mussels attach themselves to the culture substratum (rope) where they will grow up until the harvest time about 12 to 18 mo later (Mallet and Myrand 1995). However, faIl-off or slippage of mussels from sleeves may occur during the production cycle and may lead to substantial biomass losses (Grant et al. 1995, Mallet and Myrand 1995, Inglis and Gust 2003). FaU-off of mussels from sleeves can represent substantial losses of 742.3 ± 492.3 kg/day in July at the culture sites in the House Harbour lagoon (Leonard 2004). Factors inducing these faIloffs are poorly understood. As mussel attachment strength is variable (Carrington 2002b), fall-offs may be, at least partly, the result of a weaker attachment of the mussel byssus. The byssus, composed of multiple extracellular collagenous byssal threads secreted by a gland in the foot, tethers the mussel to its substratum. Byssal threads have a limited lifetime (likely 4-6 weeks) and decaying threads must be replenished (Carrington 2002b). Thus the mussel must secrete new threads regularly to stay attached to the substratum. In most of the studies on attachment strength of mussel byssus, the number of threads is used to characterize attachment strength (more threads = stronger attachment) and single explanatory factors are usually under controlled investigation (Young 1985, Lee et al. 1990, Dolmer and Svane 1994, Cote 1995, Dolmer 1998, Clarke 1999, Selin and Vekhova 2004, Alfaro 2005). In other studies, attachment strength is defined as the force a mussel needs to stay attached to its substrate. Such studies have usually been performed in field conditions on wild mussels attached to rocky shores (Price 1982, Carrington 2002b, Zardi et al. 2007).

A number of factors can influence the attachment strength of mussels in natural populations. For example, byssal thread production (and thus attachment strength) increased with water temperature ranging from 0 to 25°C, but is inhibited above 26°C (Young 1985, Lee et al. 1990, Sel in and Vekhova 2004). Food availability can also influence attachment strength by decreasing threads production when food is limited (Price 1980, Young 1985, Clarke 1999, Carrington 2002a). Mussels living in the intertidal zone are also challenged by hydrodynamic forces generated by wave action (Price 1982, Carrington Bell and Denny 1994, Bell and Gosline 1997, Carrington 2002b, Hunt and Sheibling 2002), and byssal thread production depends on various aspects of water motion, such as CUITent velocity (one-directional water motion) (Lee et al. 1990, Dolmer and Svane 1994, Bell and Gosline 1997, Alfaro 2005, Moeser et al. 2006) and turbulence (multidirectional water motion) (Mahéo 1970, Van Winkle 1970, Young 1985). CUITent velocity, which is often associated to wave action in intertidal zone, was generally used in studies to characterize the hydrodynamic forces instead of the water turbulence. In addition to exogenous factors like those cited above, endogenous factors like reproductive condition may also be linked to mussel attachment strength (Hawkins and Bayne 1985, Seed and Suchanek 1992). Several studies observed an inverse relationship between reproductive cycle ~d attachment strength, suggesting that mussels may not always have available energy for byssal thread production, specifically when gamete production occurred (Price 1980, Price 1982, Carrington 2002b, Zardi et al. 2007). Mussel attachment strength does not just depend on the number of byssal threads produced, but also on the material properties of the threads (Moeser and Carrington 2006).

MATERIALS AND METHODS:

A preliminary study was conducted in 2004 from June 25 to October 13 and this effort guided a more extensive sampling in 2005 (longer sampling season and improved monitoring of the water column characteristics). Thus the main experiment occurred from May 24 to October 17 in 2005 with attachment strength measurement, reproductive condition determination, seston characterization and environmental monitoring of the water colurnn. The less extensive data of 2004 are presented as a useful comparison.

Sile:
Experiments took place in the House Harbour lagoon in the Magdalen Islands (Quebec, Canada), where blue mussels (Mytilus edulis) are cultivated (Figure 4). The maximal depth of the House Harbour lagoon and at the experimental site is approximately  m. The lagoon communicates with the open sea by a relatively narrow channel. The maximum tidal amplitude is only about 0.5 m inside the lagoon (Koutitonsky, unpub. data). Tidal currents velocities are relatively low in the basin « 0.05 m S-I); wind is very important in mixing of the water column of this shallow lagoon (Koutitonsky et al. 2002, Koutitonsky and Tita 2006).

Individual force of byssal threads:
An additional 10 mussels were taken haphazardly from sleeves at two different dates in the summer (August 02, 2005) and faH (October 17, 2005) foHowing the attachment strength measurements. Musse! byssus was removed carefully from its substrate, thread by thread, at the plaque region of the thread and the byssus was eut off at the shell margin (corresponding to the proximal region of the thread). Byssus were then dehydrated by air exposure in an open plastic bag until tensile tests were performed (Brazee and Carrington 2006). The byssus (byssal threads and stem) of each mussel was rehydrated 30 minutes in seawater before testing. The two ends of the byssal threads (distal or dise region and proximal or stem region) were mounted within a pair of grips using cardstock and cyanoacrylate glue, which were attached to a mobile crosshead of an Instron 5565 tensometer (Instron, Canton, MA, USA) (Moeser and Carrington 2006). Threads were submerged in seawater at 15°C and extended 10 mm*minI until failure occurred. Force (± 0.02 Newtons) was recorded every second and the maximum value was used as the thread strength.

DISCUSSION:

There was an important variation of the attachment strength in suspension-cultured mussels (M edulis) from June to October 2005 in a sheltered lagoon of the Magdalen Islands with almost a two-fold increase in fall (September-October) relatively to summer. Such a two-fold increase was also measured in the preliminary experiment in 2004. Similar variation in attachment strength of wild mussels, following a seasonal cycle, has also been observed on Rhode Island shores (Carrington 2002b, Moeser and Carrington 2006), in Nova Scotia (Hunt and Scheibling 2001), in the UK (Priee 1982), and in South Africa (Zardi et al. 2007). Carrington (2002b) found a similar pattern to the present study with values of tenacity (attachment strengthlplanform are a) increasing twofold in falllwinter relatively to summer. Although the present study covered a shorter period « six months each year), it is unique for its higher sampling frequency compared to the previous studies i.e. weekly rather than monthly samplings. This higher sampling frequency provided a more precise picture of attachment strength transitions between the seasons. ln 2005, there was a very steep decline in attachment strength at the end of June (-32 % in one week) and a graduaI increase from the beginning of September until mid-October. A similar pattern was observed in 2004, although the decrease in late June is less evident because no data were collected before June 25. These results confirmed field observations in the Magdalen Islands where mussels are known to be tightly attached to the culture substrate during the spring months but very loosely attached during the summer months before gaining a stronger attachment in fall (B. Myrand, pers. obs.). The weak attachment during the summer months may thus lead to heavy fall-offs (Bourque and Myrand 2006). Therefore heavy losses in commercial production during summer are probably related to a weaker attachment strength and not solely to mortality or predation (Mallet and Myrand 1995, Myrand et al. 2000, Inglis and Gust 2003).

Factors influencing the attachment strength
In addition to water temperature, the most influential factors on attachment strength In field conditions were water turbulence (hydrodynamic conditions) and mussels reproductive condition.

Temperature seems, at first, to be the most influential factor on attachment strength because of its strong negative correlation (r = -0.79) in 2005. This parame ter is the only factor retained in the forward stepwise multiple regression model and it explained 65.5% of the variability of the attachment strength. A similar relationship was observed in 2004 (r = – 0.72) and it was the first factor entered in the multiple regression model and it explained 60.2% of the variability of attachment strength. The temperature varied between 8 to 21 °C, in 2005, during the sampling period with higher values in the summer when attachment strength was weak and lower values in the late spring and faIl when attachment strength was high. The same pattern has been observed in 2004. This inverse relationship between temperature and attachment strength is in accordanee with Carrington (2002b) for M edulis in Rhode Island. However, these results need to be interpreted with caution. First, Priee (1982) observed the opposite pattern with a positive correlation between attachment strength of M edulis and temperature on England shores where temperature varied between 10 and 15 oC, with a maximal value of 17 oC in September. Furthermore, a number of laboratory studies showed that the production of byssal threads increase with temperature within a range of 5-25°C (Van Winkle 1970, Young 1985, Selin and Vekhova 2004, Kobak 2006). This positive relationship between temperature and attachment strength (more byssal threads = higher attachment strength) was not evident in this field study, perhaps because threads decay is higher in the surnmer when temperature is warm (Carrington 2002b). Doing so, temperature could possibly have a direct negative effect on attachment strength through a higher rate of threads decay than threads production .. Further studies on threads decay would be needed for a better understanding of this negative temperature-attachment strength relationship in field conditions.

When a forward stepwise multiple regression was performed without temperature as an explanatory variable, water turbulence became the most important factor acting on attachment strength explaining 50% of its variability. This is due to the high correlation between turbulence and attachment strength (r = 0.72). Despite the missing values for the first 4 weeks at the beginning of the sampling period, turbulence followed a similar temporal pattern than attachment strength with low values in the summer and an increase in the fall. Turbulence is a hydrodynamic parameter characterizing the water column and is defined as fluid particles moving in a highly irregular manner with intense small-scale three-dimensional motion (Vogel 1989, Mann and Lazier 2006). Water motion has also been suggested to have an important influence on attachment strength of wild mussels on wave-swept shores (Priee 1982, Witman and Suchanek 1984, Bell and Gosline 1997, Hunt and Scheibling 2001 , Carrington 2002a, Carrington 2002b, Hunt and Sheibling 2002). This positive relationship was also observed in laboratory as an increase in water agitation or flow velocity triggered threads production and an increase of mussels attachment strength (Mahéo 1970, Van WinkJe 1970, Witman and Suchanek 1984, Young 1985, Lee et al. 1990, Dolmer and Svane 1994, Alfaro 2005). As suspension-cultured mussels in the present study were kept in the water column, at 2 m below the surface, it is likely that hydrodynamic parameters acting in the lagoon do not influence the attachment strength of mussels in the same way as in the intertidal zone. However, turbulence seemed to be the most influential hydrodynamic parameter on the attachment strength of mussels in the wellmixed water column of this shallow lagoon (Koutitonsky et al. 2002). Water turbulence seemed to influence the attachment strength of cultured mussels throughout most of the sampling period.

The major decrease in attachment strength occurred rapidly and almost simultaneously with the massive spawning. The decrease in attachment strength occurred anytime between June 20 and June 27 while spawning occurred somewhere between June 27 and July 4. Thus both events could have occurred almost simultaneously and a daily sampling would had been useful to better define the relationship between both factors. To our knowledge, no other studies reported such a synchrony between a sharp decrease in attachment strength and spawning. Indeed, in the open water near the Magdalen Islands, a drastic dec1ine of attachment strength and gonad index of suspension-cultured mussels occurred simultaneously (Lachance et al., unpubl. data). As threads decay usually takes about 4-6 weeks (Carrington 2002b), this sharp dec1ine in attachment strength within one week suggests that numerous threads were “Iost” in a short period of time near or during spawning. Mussels possibly sever their own byssal threads (Mahéo 1970, Price 1983, Lee et al. 1990, Hunt et Sheibling 2002) or threads decay was accelerated at this moment. After having invested large amounts of energy in the gamete production, spawning is known to be a stressful event which can weaken the mussels and even lead to massive mortality (Worrall and Widdows 1984, Mallet and Carver 1993, Mallet and Myrand 1995, Myrand et al. 2000). For example, digestives cells of the digestive tubules of mussels show disruption of their structure and evidence of autolysis after spawning (Bayne et al. 1978). This could decrease their ability for food absorption and thus limit their energy intake. As a result, less energy could be available for the production of new byssal threads for a certain period of time after spawning thus contributing to a low attachrnent strength at this moment..

Wind-turbulence relationship
Wind velocity is the major source of water turbulence (Mann and Lazier 2006) and may serve as a proxy when no turbulence data are available like in the 2004 preliminary experiment. Turbulence is an important factor driving the variation of attachment strength of mussels but its measurement is not always possible because it needs specialized equipment and specifie expertise. In 2005, the relationship between wind velocity and turbulence at the experimental site was examined. Both increased in the fall and there were important increases in wind velocity when turbulence peaked. The mixing of the water colurnn is provided essentially by wind action in this kind of shallow lagoon (Kjerfve 1994, Koutitonsky et al. 2002). Whatever its direction, wind velocity explained 50% of the turbulence measured at the experimental site near the bottom of the lagoon in 2005. As the mus sel sleeves were suspended at 2 m from the surface, we can hypothesize that the impact of the wind velocity on turbulence could be higher than measured near bottom since the effects of the wind on the particles in the water decrease with depth (Kjerfve 1994). In contrast to turbulence, wind velocity was not significantly correlated to the attachment strength of mussels in 2005. However, even if the wind velocity was not significantly correlated to attachment strength in 2004, this factor was retained in the multiple regression model explaining 6.2% of the attachment strength variability and showed a similar increase in faIl than attachment strength. This weak relationship between wind velocity and attachment strength could be probably due to the indirect impact of the wind on mussels kept suspended in the water column. Indeed, the direction of the wind could influence the impact on the mus sel sleeves. For example, southerly winds are partly blocked by the House Harbour Island. Nevertheless, wind velocity showed a general pattern similar to attachment strength in 2004 and 2005.

CONCLUSION:

In conclusion, this is the first study to examine the attachment strength of suspensioncultured mussels and also the first to study temporal changes of the attachment strength in field conditions based on weekly samplings. The attachment strength of mussels varied twofold from summer to faIl. The individual force of byssal threads also increased substantially in fall compared to summer, contributing to the increase of attachment strength. The water temperature was the factor with the highest correlation with attachment strength and this was an inverse relationship. A higher temperature could increase the byssal threads decay during the summer and then lead to a lower attachment strength. After water temperature, turbulence was the second factor with the highest correlation with attachment strength. This latter factor seemed to influence attachment strength after the massive spawning in early summer. Mussels did not attach firmly to the sleeves in the surnmer when turbulence is low, but they increased their attachment strength with the increase of turbulence in faIl to provide against their dislodgement. Reproduction seemed to have an impact on attachment strength as a mass spawning occurred almost synchronously with a major decrease in attachment strength in late June. This was the first time spawning seemed to be so closely synchronized with a major decrease in attachment strength. Wind velocity is related to turbulence and thus can provide information relatively to the influence of turbulence on the attachment strength of mussels. Mussels growers should be careful when they harvest during the spawning period and the summer period to minimize possible faIl-offs due to the weakening in mussel attachment.

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Table des matières

INTRODUCTION GÉNÉRALE 
Mytiliculture
Pertes de moules
Le byssus
BUT ET OBJECTIFS
CHAPITRE 1: BIOTIC AND ABIOTIC INFLUENCES ON THE A TT ACHMENT STRENGTH OF BLUE MUSSEL (MYTILUS EDULIS) FROM SUSPENDED CULTURE, IN THE MAGDALEN ISLAND (QUÉBEC, CANADA).
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
Site
Attachrnent strength and reproductive condition
lndividual force of byssal threads
Seston characterization
Environmental monitoring
Statistical analysis
RESULTS
Resultsfor 2004
Relationship with attachment strength (2004)
Results for 2005
Attachment strength (2005)
lndividualforce ofbyssal threads (2005)
Reproductive condition (2005)
Environrnental data (2005)
Relationship with attachrnent strength (2005)
Wind-turbulence relationship (2005)
DISCUSSION 
Factors influencing the attachrnent strength
Wind-turbulence relationship
CONCLUSION

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