Fouling Community of the Snow Crab Chionoecetes Opilio in Sydney

Cah. Biol. Mar. (2007) 48 : 347-359

Fouling community of the snow crab Chionoecetes opilio in Sydney Bight, Canada: preliminary observations in relation to sampling period and depth/geographical location

Luc SAVOIE1, Gilles MIRON2 and Michel BIRON1* (1) Centre des pêches du Golfe, Pêches et Océans Canada, C. P. 5030, Moncton, Nouveau-Brunswick, Canada E1C 9B6. * Corresponding author Gilles Miron: [email protected] (2) Département de biologie, Université de Moncton, Moncton, Nouveau-Brunswick, Canada E1A 3E9 Fax : +1 (506) 858-4542

Abstract: We examined the foulers on the exoskeleton of 498 male snow crabs (Chionoecetes opilio) sampled off the eastern coast of Cape Breton Island (Sydney Bight). A total of sixteen sessile invertebrate families were identified. The most dominant families belonged to the bryozoans (Alcyonididae and Hippothoidae), the cirripeds (Balanidae) and the polychaetes (Spirorbidae). Crabs hosted different fouling communities in relation to depth/geographical locations and sampling periods. These differences were confirmed by multivariate analyses (e.g., MDS plot, ANOSIM and SIMPER analyses). The fouling communities observed on crabs sampled at depth > 150 m significantly differed from those from < 150 m. These differences were mainly caused by the presence of the bivalve Anomia sp. (Anomiidae) and cocoons from the Hirudinae Johanssonia artica (Piscicolidae) over 150 m. The fouling communities sampled in September 2001 and October 2002 were significantly different than those sampled during the other periods. The similar fouling communities observed in the Sydney Bight at depths < 150 m may be related to the mobility of the snow crabs in the top 150 m.

Résumé : Communauté d’épibiontes du crabe des neiges Chionoecetes opilio au large de Sydney Bight, Canada : observa- tions préliminaires en fonction de la période d’échantillonnage et de la profondeur/région géographique. Nous avons examiné les épibiontes retrouvés sur l’exosquelette de 498 crabes des neiges (Chionoecetes opilio) mâles échantillonnés au large des côtes de l’Île-du-Cap Breton (Sydney Bight). Seize familles d’invertébrés sessiles ont été identifiées. Les familles les plus importantes appartenaient aux bryozoaires (Alcyonididae et Hippothoidae), cirripèdes (Balanidae) et polychètes (Spirorbidae). La communauté d’épibiontes observée sur les crabes variait en fonction de la profondeur et de la période d’échantillonnage. Ces variations sont confirmées par des analyses multivariées (e.g. analyses MDS, ANOSIM et SIMPER). La communauté d’épibiontes observée sur les crabes échantillonnés à plus de 150 m était significativement différente de celle des crabes échan- tillonnés à moins de 150 m. Ces variations étaient principalement causées par la présence du bivalve Anomia sp. (Anomidae) et de cocons de l’Hirudinae Johanssonia artica (Piscicolidae) à des profondeurs supérieures à 150 m. Les communautés d’épibiontes observées en septembre 2001 et en octobre 2002 étaient significativement différentes de celles observées lors des autres périodes d’échantillonnage. La similarité des communautés observées dans Sydney Bight aux profondeurs inférieures à 150 m peut être attribuée à la mobilité des crabes dans les premiers 150 m de profondeur.

Keywords: Snow crab l Chionoecetes opilio l Fouling community l Distribution l Variability l Atlantic Canada

Reçu le 14 mars 2007 ; accepté après révision le 20 août 2007. Received 14 March 2007; accepted in revised form 20 August 2007. 348 FOULING COMMUNITY OF THE SNOW CRAB CHIONOECETES OPILIO

Introduction hardness, and the general abundance of epibionts (Moriyasu et al., 1998). The snow crab, Chionoecetes opilio (O. Fabricius, 1788), is Epibiosis is a common life-history strategy observed a subarctic species found in the Atlantic Ocean from among marine organisms (Wahl, 1989). It involves mutual Northern Labrador to the Gulf of Maine and in the Pacific and commensal relationships between a fouling species and Ocean (Powles, 1968; Tremblay, 1997). Individuals from its host with the most critical factor being the availability of the southern Gulf of St. Lawrence (SGSL) bearing a a suitable substratum (Moldonado & Uriz, 1992; Parapar et carapace width > 40 mm generally molt once a year and are al., 1997) and the presence of various chemical, physical characterized by a terminal molt (Moriyasu et al., 1987; and biological parameters (Wahl, 1989). Decapod Conan et al., 1988). The adult males generally prefer crustaceans may provide such a suitable substratum for muddy habitats over a broad range of depths (20 to 400 m) settlers, and although they may not show a high degree of where low temperatures are observed (-1 to 3°C) (Chassé et colonization, most of them support many invertebrates al., 2004). The snow crab is considered as a sedentary (Parapar et al., 1997; Fernandez et al., 1998). The exoskele- species (Watson, 1970) but may exhibit seasonal migrations ton of snow crabs, once the terminal molt has been in some areas for molting and mating (Ennis et al., 1990; completed, offers a microhabitat for epibiotic organisms. Sainte-Marie & Hazel, 1992). The fouling community may vary in time and geo- The snow crab fishery relies, in part, on the age structure graphically. Results from Dick et al. (1998) and Savoie et of the stock to define fishery management strategies. Age is al. (2007), for instance, showed that the structure of the estimated from a carapace stage chart that is based on fouling community differed between regions for two crab carapace condition. This classification was developed for species of the genus Chionoecetes. The fouling community the SGSL and considers factors such as color, wear, may thus represent a habitat signature depending on the

Figure 1. Location of study site. Figure 1. Localisation du site d’étude. L. SAVOIE, G. MIRON, M. BIRON 349 amount of time a crab spends under a given set of environ- Bight is characterized by a rocky shallow shelf near the mental parameters (e.g., depth, temperature) (Key et al., coast and an offshore muddy bottom. It is bordered on the 1997). The colonization of a substratum depends on the east by a 500 m deep trench, the Laurentian Channel. It is abundance of settling larvae, which in turn is a function of an area where cold, muddy substrates occur over a broad the habitat selection behaviour and the season. The range of depths. evolution of the fouling community also depends on the fouling history and the presence/absence of a dominant Sampling species (Osman, 1977). Crabs were collected with a Bigouden Nephrops trawl The aim of this study was to describe the variability of (Conan et al., 1994) hauled by a 20 m stern-trawler the fouling community observed on the exoskeleton of chartered by the Department of Fisheries and Oceans snow crabs in relation to the sampling periods and (DFO) for the annual assessment of the snow crab stocks depths/geographical locations and provide a comparative (Biron et al., 2002 & 2003). The fouling community was data set of foulers to fishery stakeholders. described using the exoskeleton of 498 adult male snow crabs. Only male crabs were used since the fishery relies on Material and Methods carapace information from males. Crabs were collected in September 2001 (S1) and May (S2), July (S3) and October 2002 (S4). Thirty stations were sampled per sampling Study area period with a maximum of 6 adult crabs (when available) randomly collected per station (Fig. 2). The location of the Snow crabs were collected from the Sydney Bight off the trawl station within each 10 minute latitude/longitude grid eastern coast of Cape Breton Island (Fig. 1). The Sydney

Figure 2. Location of sampling stations for each sampling period (I < 75 m; G 75-150 m; L > 150 m). Figure 2. Répartition des sites d’échantillonnage lors de chaque période d’échantillonnage (I < 75 m ; G 75-150 m ; L > 150 m). ) 5 7 8 7 5 5 0 0 0 0 3 3 0 0 2 0 ...... 4 ...... 7 1 0 1 7 2 2 0 0 0 0 8 8 3 0 4 0 0 3 4 7 9 3 6 = D N ( ) 7 3 3 5 0 5 2 8 0 7 5 0 2 0 8 0 5 8 8 ...... 2 2 3 3 7 7 5 4 7 = 0 D 8 3 0 1 8 0 1 8 3 9 1 7 1 1 8 N ( ) 6 0 5 3 2 2 8 9 3 6 . 2 0 0 7 1 0 0 7 7 ...... 0 1 2 6 6 0 6 2 4 = 0 0 D 7 0 7 7 0 0 1 9 4 9 3 7 4 3 1 N ( ) r 7 e 0 2 8 2 3 5 8 2 6 8 0 b 9 0 1 0 5 0 8 5 ...... 0 ...... o 7 2 8 3 6 8 0 7 5 0 t 1 0 7 0 2 6 = 0 c 1 8 3 9 1 6 2 1 8 2 N O ( ) 8 2 7 6 1 1 7 9 3 0 3 0 0 0 6 0 0 0 1 ...... 350. FOULING COMMUNITY OF THE SNOW CRAB CHIONOECETES OPILIO = 5 8 2 2 0 2 4 0 0 D 0 7 0 3 0 0 0 3 7 3 8 1 4 1 5 N ( s n a ) d 9 e 5 6 4 4 6 1 9 7 u 2 0 0 5 0 4 7 7 1 1 ...... q = 8 6 5 6 6 1 9 i D 8 0 3 1 1 5 5 0 0 h 1 8 2 9 6 1 7 p N . ( a a r e g r ) a o é 0 t 0 0 g h 3 3 . 7 . 7 3 3 0 3 7 g 1 0 3 0 3 3 7 ...... n i ...... 0 0 = o 3 6 6 3 3 0 3 6 B D i 0 0 6 0 3 0 3 3 1 3 1 1 8 1 1 8 g y N 1 1 é ( e r / n r d ) u y 7 e S d 1 2 4 0 9 0 0 8 4 y n e 1 0 6 9 9 5 9 8 8 1 ...... l 0 o ...... h f t 1 8 9 4 5 2 4 u 0 8 0 6 2 0 6 5 = 0 0 o J 2 8 2 9 6 1 7 2 n r i p N n t ( e o i t t n a e c ) o 6 m l 0 8 3 3 8 8 5 5 0 8 5 . e 1 l 0 3 3 3 0 3 ...... v a . . . . . 0 è 8 1 6 3 8 2 2 0 8 2 c = l 0 D i 6 6 0 0 6 é 1 8 5 9 1 1 1 5 1 1 h r 1 N p p ( a r e g d ) o 1 e e d 7 7 6 4 3 g 7 / 0 2 0 0 6 0 9 2 6 9 0 2 . . . . . o ...... i h 1 2 8 3 0 = r t 0 D 7 4 0 5 0 9 5 9 4 0 é p 8 1 9 6 8 p e N d ( e u d q n ) a a 9 0 h 6 0 . 3 3 3 3 d 2 c 0 1 9 0 0 9 4 4 4 4 ...... o ...... 0 r i 6 1 9 0 0 9 = r u 0 D 6 0 0 3 3 0 3 3 6 e 9 3 7 1 1 7 o 1 p N p ( g o i n ) l i i l 6 p p 1 2 o 3 3 3 5 y 3 8 m 7 0 8 1 4 6 6 0 6 2 7 ...... 0 s a . . . . . a . . . . . e 5 3 8 5 0 2 s 0 t 1 0 7 3 2 8 5 6 1 8 = M e 8 2 9 6 1 8 2 h c c N e a ( o e n r o o i f h o C i ) l i u 7 p d 8 4 0 9 6 8 1 3 o 0 4 0 0 3 0 0 0 7 4 ...... e ...... t s 0 8 7 1 1 6 1 = t 0 5 0 0 D 0 0 e 2 0 5 e t 1 7 2 9 2 5 8 l e N e c ( u e q o s ) n o 6 o 0 x i 2 8 . 5 6 1 1 7 e h 0 3 0 3 2 0 0 9 3 6 ...... ’ ...... 0 l C 4 5 4 7 7 6 = 0 1 0 1 D 0 0 r 7 0 1 6 f 8 1 1 7 1 9 u o 1 N s ( n ) o t % ) ( e l 5 0 s e 9 9 . 3 2 4 6 6 4 e k 0 0 0 0 1 0 0 4 4 t ...... s ...... 0 n 8 8 3 2 4 5 5 = o 0 0 0 0 D 0 0 4 0 4 o x i 8 2 1 8 2 1 9 e 1 b N i ( e p r h é ) t e s 8 n b e 5 1 o 2 2 1 4 1 2 4 d 0 9 0 6 1 0 0 6 0 9 ...... m ) 0 ...... n e 4 2 8 1 4 5 2 0 0 1 0 0 t 0 0 o % 7 7 = 8 i ( 8 2 9 1 7 1 9 2 t p i s ) e r N r s a ( a e S l p n c . . . u p i t o . p t p a o h ’ f o s p c p g . d c . i r f s p . . e . a p o e p s e e a B o p i a p p . . a a . p c a p . r e l p C s y p d s p a n p d l e c p s . d m ( p a e e i s i . e e s s i i e n a l l p e e p s e p a n a r u r a a p u n l l a e r l . e a s i . s d a a d e a r p a a d q s a l e o d e o e i a m a p r o l p d r y l d a i d é s r e e r d i s s r e s c l i e i e s h r u d i i u s n d i a p o S a u t o d a a o s o d u i e o n i a c i r i a o n a F e r a e n t a i b i i a l o p l i r n i c d o p a u d h n p i a c n p o a . e d d p i o e o b i z t r i i i o i l e n m o u d o i a d m i i o e p 1 a O a i o l a r a t l p d l u b p y s a l r n l e o o z o i e c l l o c p g i l s l n o p i . i i p o z i h y r h i o e o m c u u h a b e i i p p n l o r e a r n e e y 1 n a v n l a l l p a r u p c c z c o o l d a l l t b m c i l l l o r i o h p p c r e e o s J A S B H O L C S S A H C C C A C r n a o i i e l u a a e a a r u l l i y p c c i x d y l r b b r v v a P S A B H S T C N S H H C C A A i y i i r o a a n T e T T H P B C H B s e l L. SAVOIE, G. MIRON, M. BIRON 351 was chosen using a systematic random sampling design test (Clarke, 1993) was used to compare similarities in (Biron et al., 2002 & 2003). The number and location of family compositions between samples. A two-way nested stations were based on the available depth range and ANOSIM was performed with the transformed data to test geographical coverage: < 75 m around Smokey Bank (D1), differences between the four sampling periods and the three 75 to 150 m in the main fishing area (D2), > 150 m near the depth/geographical locations. Similarity of percentages slope of the Laurentian Channel (D3) (Fig. 2 and Table 1). analysis (SIMPER) was used to determine which family At each location, temperature (Minilog® sensor), depth contributed the most to any dissimilarity among sampling (depth sounders) and position (DGPS system) were taken. periods and depth/geographical locations (Clarke & Each crab collected was bagged and frozen individually Warwick, 1994). and brought back to the laboratory for analysis. Finally, richness (number of families) was used as a community index. Values were compared among sampling Laboratory periods and depth/geographical locations using a one-way Carapace width (CW), carapace length (CL) and chela ANOVA. Data were log (1+x)-transformed to obtain homo- height (CH) were measured in all crabs with a digital geneity of variances. Multiple pairwise-comparison tests, using least-square means, were performed for post-hoc vernier caliper (Conan & Comeau, 1986). These parameters comparisons after all ANOVAs, using the Tukey test. were used to insure that crabs reached their terminal molt. Homogeneity of variances was tested with the F-test and Crabs were categorized using the carapace stages from normality of data was evaluated by examining plots of the Moriyasu et al. (1998). The dorsal, ventral and limb residuals. If transformation of the data did not lead to external surfaces of the carapace were examined for epi- homogeneity of variances, no statistical test was conducted. biotic coverage on each crab. The type, location and ANOVA and post-hoc comparisons were carried out with number of foulers were noted. Although foulers were SYSTAT 9.0©. identified to the genus or, whenever possible, to the species, only the family was used in the analyses due to a small number of individuals for certain genera. Counts were Results made for solitary individuals. Epibiotic families occurring in 10% or less of crabs were considered minor families while the ones occurring in 50% or more were considered General observations major. Abundance determination for colonial animals was Sixteen sessile invertebrate families were observed on the made differently depending on the species. For the colonial exoskeleton of crabs (Table 1). These families were bryozoans Alcyonidium spp., estimated percentage distributed amongst six phyla. Occurrences of each coverage was recorded for each of the crab’s external identified family (as well as the genera) are shown in Table surfaces (dorsal, ventral and side legs). A count of 1 1, where percentages are presented for each sampling individual was given to Alcyonidium spp. in the case of a period and each depth/geographical location. Overall, no surface coverage of 10% (Dick et al., 1998). The ≤ general pattern was observed amongst the minor families. estimated percentage coverage was divided by 10 and Minor families were more numerous on the exoskeleton of rounded to the nearest whole number to give the number of crabs during the summer period (nine in May and eight in individuals in cases where surface coverage exceeded 10%. July 2002) than during the fall (five in September 2001 and Each separate colony of bryozoans other than Alcyonidium four in October 2002). Four families had major occurrences spp. that did not generally form extensive merging colonies in each of the sampling periods: Balanidae cirripeds was recorded as 1 individual. The identification of certain (98.1%), Alcyonididae (92.4%) and Hippothoidae bryozoan families was confirmed by the Atlantic Reference bryozoans (74.1%) and Spirorbidae polychaetes (84.2%). Centre (ARC), St. Andrews (NB), Canada. These families were also observed on crabs sampled at each depth/geographical location. Bryozoans from the Aeteidae, Statistical analysis Schizoporellidae and Scruporellaridae families appeared Multivariate analyses were used to study the fouling more frequently on crabs during the sampling periods in the assemblages including multi-dimensional scaling (MDS), summer than the ones in the fall. Members of the analysis of similarities (ANOSIM) and similarity Celleporidae family appeared more frequently on crabs percentages (SIMPER). These analyses were carried out sampled during the sampling periods in the fall. with PRIMER 5©. MDS were based on Bray-Curtis Occurrences of the Alcyonididae, Hippothoidae, Balanidae similarities. Data (number of each epibiont per crab) were and Spirorbidae families decreased from shallow (< 150 m) transformed (fourth root-transformation) to minimize bias to deep waters (> 150 m), except for the Alcyonididae from highly abundant families. The ANOSIM significance family during the May 2002 sampling. 352 FOULING COMMUNITY OF THE SNOW CRAB CHIONOECETES OPILIO

Figure 3. Relative abundance (%) of phyla observed on male snow crabs (Chionoecetes opilio) for each depth/geographical location (D1: < 75 m; D2: 75-150 m; D3: >150 m) and sampling period (S1: September 2001; S2: May 2002; S3: July 2002; S4: October 2002). All sampling stations are confounded in pie charts for each sampling period (left column). Figure 3. Abondance relative (%) des phyla observés sur les crabes des neiges (Chionoecetes opilio) mâles à chaque profondeur (D1 : < 75 m ; D2 : 75-150 m ; D3 : > 150 m) et période d’échantillonnage (S1 : septembre 2001 ; S2 : mai 2002 ; S3 : juillet 2002 ; S4 : octobre 2002). Toutes les stations d’échantillonnage sont confondues dans les graphiques pour chaque période d’échantillonnage (colonne de gauche).

The relative abundances for all families (as well as the were usually higher at depth > 150 m compared to those genera) are presented in Table 2 for each sampling period observed at depths < 150 m. Temperatures closest to the and depth/geographical location. Differences were mainly water surface (< 75 m) were colder in May 2002 and limited to three families for the sampling periods: increased as the year progressed. Temporal variations in Balanidae, Spirorbidae and Hippothoidae. The Balanidae water temperatures were less important at depths > 75 m. family was the dominant one. The Spirorbidae family increased steadily from September 2001 to October 2002. Multivariate analyses Most of the bryozoan families were rare and made no Two apparent groups were revealed by the MDS analysis significant difference in the family composition found on based on the assemblage of the fouling community (Fig. 4). the crabs. The Anomidae family (bivalve) increased from The first group is related to crabs sampled in September shallow to deep waters. The same pattern was observed for 2001 (S1) whereas the second cluster is related to crabs cocoons from the Piscicolidae family (Hirudinae). Figure 3 sampled at depths > 150 m (D3). Results from a two-way illustrates the variations observed in the relative abundance crossed analysis support that sampling period (R = 0.115, of the six major phyla. P < 0.001) and depth/geographical location (R = 0.08, Temperatures varied with the sampling periods and P < 0.001) significantly affected the fouling community. depth/geographical locations (Table 3). Water temperatures The pair-wise test showed a similarity in the fouling ) 5 9 0 0 0 0 3 3 0 0 0 9 7 8 7 . . . 4 ...... 9 3 0 2 0 0 0 0 0 3 7 0 0 0 5 1 0 1 5 1 = D N ( ) 7 7 7 5 2 0 0 0 8 3 6 4 7 8 2 5 3 7 ...... 7 7 = D 1 0 0 0 0 0 1 6 0 0 0 1 0 3 4 N ( ) 6 0 2 2 0 1 1 0 0 0 0 2 2 7 3 3 6 5 ...... 4 2 = 0 0 D 2 0 0 0 4 0 4 0 0 1 0 5 3 N ( ) r 7 e 0 2 5 5 b 2 1 0 0 8 1 5 4 8 7 1 5 4 4 . . 0 ...... o 1 2 0 t 0 2 0 0 0 2 1 5 0 0 0 = 1 0 c 4 4 2 N O ( ) 8 2 0 7 0 3 0 0 0 0 8 1 6 7 4 5 5 5 ...... = 7 1 0 D 5 0 0 0 0 7 4 0 0 0 1 0 1 6

N L. SAVOIE, G. MIRON, M. BIRON 353 ( ) s 9 e l 5 3 2 2 0 0 0 3 1 6 6 1 2 2 1 3 8 . . s ...... = n 7 5 D a 2 0 0 0 0 4 1 6 0 0 0 1 0 2 5 . d N a ( e e r u a q ) i t 0 h h p 3 g 1 9 i a 1 0 7 3 4 4 7 2 8 1 2 4 5 1 . . r ...... B = 6 6 g D 3 0 0 0 2 0 0 6 0 0 0 1 0 o y 3 4 é e N ( g n d n y ) o i S 7 g 1 n 2 é 4 6 i y r 1 0 0 0 4 2 6 2 6 6 1 1 4 6 . . l 0 / ...... n r 8 3 u 0 o u 3 0 0 0 1 3 0 6 0 0 0 = 1 0 J i 2 5 2 e t d a N c n ( o o l f l o r a ) p c i 6 t h e 0 5 8 1 p 3 0 0 3 2 4 4 8 1 6 3 5 2 . . . t a ...... n r 9 3 0 = D e 0 0 6 1 1 0 3 0 0 0 2 0 g 2 4 1 o m N e e ( g v / è h l ) t é p 1 r e 6 6 p 7 d 2 0 0 8 3 8 1 3 0 1 2 1 3 6 ...... e 6 0 d = d D 1 0 0 0 1 0 6 0 0 0 0 1 0 n 2 6 e a N d ( d o i o r i r ) é e p 9 p 0 1 7 2 e 1 0 0 5 1 1 4 1 1 2 3 6 1 . . . g u ...... n 8 5 0 = q i D 2 0 0 0 0 0 0 0 0 0 1 0 l a 2 5 1 p h N c ( m r a ) u s o 6 h p 1 c 2 2 2 y a o 1 2 1 1 1 0 3 8 4 9 1 2 3 7 . . 0 a i . . . . e ...... l 7 7 0 i r 0 0 0 0 3 1 0 0 6 0 0 0 = 1 p M 2 5 o 2 f o N s o ( i e l t i e p c o e o s e n ) t o 7 e i c 9 h 3 e 0 0 1 1 3 0 9 5 7 1 6 3 1 8 . 0 . . . . . C ...... o . 6 = n 0 0 0 0 D 0 1 6 0 0 0 2 0 0 u 0 8 o d i N h e ( t t C e f ) l o e 6 u 7 n 7 q 0 0 0 0 2 0 0 6 8 7 4 1 1 1 . o 3 ...... s t . 6 = o e 0 0 0 0 D 0 0 5 0 0 0 4 0 1 l 0 x 8 e e N ’ k ( l s r o u x ) s e 5 s e 7 4 e 0 0 0 0 1 0 0 4 4 1 2 1 1 6 . h t 3 ...... t . 1 n = 0 0 0 0 D 0 4 0 0 0 2 0 0 0 n o 0 9 i o N b i s ( r p r e ) é l e 8 u s b e o 5 1 f 8 d 0 0 0 0 1 0 8 4 4 3 2 9 3 1 8 . m 0 f ...... ) e 8 o 0 0 0 0 0 0 t 0 5 0 0 0 2 0 0 = 0 % ) 8 2 ( p ) e % N e ( s ( a v S i n e . c t . c i a o . p t p l n e o s p p c a r . c . r . s d p . . t e . a p e e n p s e a o h p i a c p p . a a u . p a p . r g l n p C s b d s p i a p d l p s . d m a ( p a e i s i a . e s i i e B l l p e e p s d e p a a r u a r a p n l l a e r l . e a s i n . s a a e a y . a p a d s l a e o d v e e o a a p o o l p d r l d e i a i d s r e p r e d i s s e l s c i t e i e s h b d i i s n n d i a p o a s u t o a d a o a o s d u e n i a i r i a o n a e r a e n d l t a A i b i i a l o p l i r n i d o p a d h p n i a e n o a y e d d p i o . e o i b z t r i i i o l i e n m u o o a m d m o i i p a S o i a l 2 a R r a t l p d l u b p y s a r n e o o z o i e c l l o c g p i u l l p n o i i i p o z . i h y r h o i e o m c u i u h b i e i p p n l e o r a r e y e n v a n l a l l 2 p a r u p c c z d o c l o d a l l t m c c i l l l r i o h p p c r o s e e A S B O L C S A J S H C C C A C n a o i i l e s e u a a e a a r l l y p i c c x d l n y l r r b b v a S A P S S B H N C H H C C A A i y o a i i r o a a r i T T T P H B H C H B v n e 354 FOULING COMMUNITY OF THE SNOW CRAB CHIONOECETES OPILIO

Table 3. Water temperature (mean ± 95% confidence interval) observed for each depth during the sampling periods. Tableau 3. Température de l’eau (moyenne ± int. de conf. à 95%) observée à chaque profondeur pendant les périodes d’échantillonnage.

Sampling period Depth (m) Temperature (ºC)

< 75 2.17 ± 0.12 September 2001 75-150 1.81 ± 0.13 > 150 5.18 ± 0.29 < 75 0.15 ± 0.06 May 2002 75-150 1.56 ± 0.22 > 150 4.35 ± 0.78

< 75 1.19 ± 0.15 Figure 4. Two dimensional MDS ordination of sampling July 2002 75-150 1.84 ± 0.12 period-depth/geographical location strata by the Bray-Curtis > 150 5.26 ± 0.33 dissimilarity of the 4th root transformed abundances of all < 75 2.72 ± 1.34 members of each family. D1: < 75 m; D2: 75-150 m; D3: >150 m; October 2002 75-150 2.08 ± 0.12 S1: September 2001; S2: May 2002; S3: July 2002; S4: October > 150 4.45 ± 0.43 2002. Figure 4. Représentation 2D de l’ordination MDS effectuée sur l’abondance des membres de chaque famille en fonction de la profondeur et de la période d’échantillonnage. D1 : < 75 m ; D2 : Table 4. Results from pair-wise ANOSIM tests carried out on 75-150 m ; D3 : > 150 m ; S1 : septembre 2001 ; S2 : mai 2002 ; the similarity of the fouling community between male snow crabs S3 : juillet 2002 ; S4 : octobre 2002. (Chionoecetes opilio) sampled for each sampling period and depth. Tableau 4. Résultats de l’analyse ANOSIM effectuée sur la similarité des communautés d’épibiontes observées sur les crabes sampled at the other two depths (Table 4). The absence of a échantillonnés à chaque profondeur lors des périodes noticeable effect from the sampling periods (other than S1) d’échantillonnage. and depth/geographical locations (other than D3) is clearly evident in Figure 4. Groups The SIMPER analysis revealed that the Balanidae, (Pairwise Test) R Statistic P Spirorbidae and Hippothoidae families were the main families responsible for the similarity in the fouling Depths/geographical locations community structure for each depth/geographical location D1, D2 -0.020 0.775 D1, D3 0.121 < 0.001 and that the Anomidae and Piscicolidae could be responsi- D2, D3 0.183 < 0.001 ble for the dissimilarity between deep (D3) and shallow Global Test 0.080 < 0.001 (D1 and D2) waters (Table 5A). For the sampling periods, the families Balanidae, and Spirorbidae were the main Sampling periods families responsible for the similarity in the fouling S1, S2 0.155 < 0.001 community structure, but the number of individuals S1, S3 0.181 < 0.001 observed from the family Balanidae in September 2001 S1, S4 0.240 < 0.001 S2, S3 -0.002 0.567 (S1) is largely responsible for the dissimilarity between the S2, S4 0.020 0.047 sampling periods (Table 5B). S3, S4 0.058 < 0.005 The ANOVAs carried out on the total abundance of the Global Test 0.115 < 0.001 four major phyla showed that sampling period and depth/geographical location had significant effects on cirripeds and bivalves (Table 6). The abundance of communities between crabs sampled in May (S2) and July cirripeds was greater on crabs sampled in September 2001 2002 (S3) and between crabs sampled in May and October (Fig. 5, Table 7). Cirriped abundances also varied between 2002 (S4) (Table 2). The similarity observed on crabs depths. Bivalves were more abundant on crabs sampled in sampled between depths < 75 m (D1) and depths of 75- May 2002. This relationship was due to a large number of 150 m (D2) was significant, but crabs sampled at depths individuals found on crabs sampled at depths > 150 m. The > 150 m (D3) had fouling assemblages different from crabs Tukey multiple comparison tests did not find any L. SAVOIE, G. MIRON, M. BIRON 355

Table 5. Contribution of families to similarity (%) for the fouling community observed on male snow crabs for each depth (A) and sampling period (B). Contribution to dissimilarity (%) between depths and sampling periods are also shown. Tableau 5. Contribution de chacune des familles (%) à la similarité des communautés d’épibiontes observées sur les crabes pour chaque profondeur (A) et période d’échantillonnage (B). Les contributions à la dissimilarité (%) entre chaque profondeur et période d’échantillonnage sont également montrées.

A. Depth Family Contribution to similarity (%) Contribution to dissimilarity (%) < 75 m 75-150 m > 150 m D1-D2 D1-D3 D2-D3 (D1) (D2) (D3)

Balanidae 69.21 76.32 73.80 58.06 59.76 57.87 Spirorbidae 20.07 13.58 15.33 24.98 20.93 19.81 Hippothoidae 5.90 5.21 2.98 5.82 5.47 5.77 Alcyonididae 3.78 4.28 3.54 3.52 3.09 3.97 Anomidae 0.68 0.33 2.93 2.60 4.38 5.21 Piscicolidae 0.07 0.12 0.07 1.26 2.91 4.09

B. Sampling period Family Contribution to similarity (%) Contribution to dissimilarity (%) Sept. 2001 May 2002 July 2002 Oct. 2002 (S1) (S2) (S3) (S4) S1-S2 S1-S3 S1-S4 S2-S3 S2-S4 S3-S4

Balanidae 89.96 73.77 66.38 57.79 71.72 71.64 65.86 44.80 39.82 38.82 Spirorbidae 4.61 17.11 20.67 28.63 14.12 13.55 20.36 28.35 35.55 35.15 Hippothoidae 2.58 5.20 6.24 5.85 4.83 4.32 4.24 8.14 7.70 7.12 Alcyonididae 2.52 3.18 4.55 5.70 3.23 3.18 3.07 4.66 4.77 4.82 Anomidae 0.18 0.52 1.15 1.29 2.42 2.60 2.29 5.34 4.69 5.00 Piscicolidae 0.03 0.11 0.77 0.23 1.35 2.23 1.26 4.33 2.55 3.85 significant differences in regard to the sampling period. The converge along the slope of the Laurentian Channel to abundance of both polychaetes and bryozoans was a create temperature and salinity gradients. Our results tend function of the interaction between sampling period and to support that the water masses in Sydney Bight vary with depth/geographical location (Table 6). Polychaetes were depth/geographical location. Water temperatures, for more abundant on crabs sampled in October 2002 (Fig. 5, instance, varied from 1.6 ± 1.9°C in depths < 75 m to 4.9 ± Table 7). This was particularly true for crabs sampled at 1.2°C at depths > 150 m. This variation may be important depths < 75 m. Polychaetes, cirripeds and bryozoans were enough to induce differences in the fouling community near usually more abundant on crabs sampled in shallow waters. the Laurentian Channel. The higher temperature of the No pattern was observed for bivalves, but they were water near the channel could increase the settlement and generally more abundant at depths > 150 m. No statistical growth of different species of larvae, increasing the number analysis was carried out for the Hirudinea and Hydrozoa of species at depth > 150 m (Table 1). taxa because of homogeneity problems. Although the snow crab from the eastern coast of Canada is traditionally described as sedentary (Watson, Discussion 1970), recent tagging studies have shown that adult males may wander over great distances. Biron (unpublished data) observed that crabs off the coast of Nova Scotia may travel Environmental conditions such as salinity, temperature and over 23 km within 3 months. In his study, only 11% of current regimes usually help define the habitat in which crabs were recaptured within 10 km of the release site on certain species may live or settle in a marine environment the Scotian Shelf, whereas over 50% of crabs were (e.g., Crisp, 1974; Key et al., 1997). The similarity between recaptured within the same distance in the southern Gulf of the fouling communities observed on snow crabs sampled St. Lawrence. The retention rate for the Sydney Bight area in the top 150 m of water may suggest that the Sydney was even lower than the one observed on the Scotian Shelf Bight area has homogeneous environmental conditions in (Biron, unpublished data). The facts that the majority of this water layer. The area is however known to be a physi- crabs from Sydney Bight are actively moving between cally complex and dynamic area (McLellan, 1954). Waters areas tend to support that they may have shared a common from the Gulf of St. Lawrence and the Labrador Current 356 FOULING COMMUNITY OF THE SNOW CRAB CHIONOECETES OPILIO

Figure 5. Number of foulers (mean ± 95% confidence interval) observed on male snow crabs in relation to depth/ geographical location and sampling period. Figure 5. Nombre d’épibiontes (moyenne ± intervalle de conf. à 95%) observé sur les crabes des neiges mâles en fonction de la profondeur et de la période d’échantillonnage. L. SAVOIE, G. MIRON, M. BIRON 357

Table 6. Summary of two-way ANOVAs examining the effect of depth and sampling period on the abundance of four major phyla found on male snow crabs. Tableau 6. Résumé de l’ANOVAà deux facteurs examinant l’effet de la profondeur et de la période d’échantillonnage sur l’abondan- ce des quatre principaux phyla retrouvés sur les crabes des neiges mâles.

Source of variation SS df MS F P

Cirripedia Sampling period 34.35 3 11.45 54.58 < 0.001 Depth/Geographical location 4.90 2 2.54 11.69 < 0.001 Sampling period X Depth/ Geographical location 1.63 6 0.27 1.30 0.256 Error 101.94 486 0.21 Total 497

Polychaeta Sampling period 5.82 3 1.94 7.39 < 0.001 Depth/Geographical location 9.62 2 4.81 18.34 < 0.001 Sampling period X Depth/Geographical location 4.13 6 0.69 2.62 0.016 Error 127.47 486 0.26 Total 497

Bivalvia Sampling period 0.88 3 0.29 2.89 0.035 Depth/Geographical location 2.69 2 1.34 13.19 < 0.001 Sampling period X Depth/Geographical location 0.59 6 0.10 0.97 0.447 Error 49.50 486 0.10 Total 497

Bryozoa Sampling period 0.28 3 0.09 0.82 0.481 Depth/Geographical location 5.77 2 2.88 25.63 < 0.001 Sampling period X Depth/Geographical location 1.64 6 0.27 2.43 0.025 Error 54.68 486 0.11 Total 497 environment at one point. Crab movements within the top on host may be important between the cirripeds and the 150 m of water in the Sydney Bight may homogenize the polychaetes. fouling communities found on crabs sampled at these The development of an abundant and diversified fouling depths. Other studies have also suggested that crabs may community on the exoskeleton should be important for wander from one region to another (Brêthes et al., 1987) ageing this species because brachyuran crabs do not exhibit increasing the similarities between the fouling many specialized body grooming structures (Bauers, 1981). communities. However, the behaviour of the crab may contribute to the The sampling period played a major role in the type of foulers observed on its carapace. Burying, for abundance of each member of the fouling community. A instance, may reduce the incidence of certain foulers large number of small barnacles were observed on crabs (Barnes & Bagenal, 1951; Abello et al., 1990; Becker, sampled in September 2001. Polychaetes were abundant on 1996). Becker (1996) showed that crabs inhabiting muddy crabs sampled in October 2002 while mollusks peaked on bottoms were significantly less densely colonized than crabs sampled during the summer sampling period of 2002. hard-bottom species. This supports the idea that crabs The colonization of a substratum is known to be dependent found in different habitats should host different epibiont upon the abundance of settling larvae, which in turn is a communities. The low number of hydrozoans found on function of the time of the year as well as the behaviour of snow crabs may reflect the burying behaviour of the snow the larvae (Osman, 1977). In the present study, the crab (Miller, 1975). sampling period and the habitat selection behaviour of It is difficult to confirm if annual or seasonal changes in some larvae could have played a role in the abundance the physical environment can cause any important variations of cirripeds, mollusks and polychaetes on snow variations in species composition on snow crabs since the crabs. Our results also tend to show that spatial competition host crabs are mobile substrata whose movement is dictated 358 FOULING COMMUNITY OF THE SNOW CRAB CHIONOECETES OPILIO

Table 7. Tukey multiple comparison tests carried out on the would like to thank H. Benoît and M. Mallet for their help abundance of four major phyla found on male snow crabs for each regarding the statistical analyses. G. Pohle (Atlantic depth (A) and sampling period (B). D1: < 75 m; D2: 75-150 m; Reference Centre, St. Andrews, NB, Canada) confirmed the D3: >150 m; S1: September 2001; S2: May 2002; S3: July 2002; identification of some Bryozoan species. We finally wish to S4: October 2002. thank M. Moriyasu and C. McKindsey for reviewing earlier Tableau 7. Tests de comparaisons multiples (test de Tukey) effectuées sur l’abondance des quatre principaux phyla retrouvés drafts of the manuscript. Comments from two anonymous sur les crabes des neiges mâles pour chaque profondeur (A) et reviewers also improved the manuscript. période d’échantillonnage (B). D1 : < 75 m; D2 : 75-150 m ; D3 : > 150 m ; S1: septembre 2001 ; S2: mai 2002 ; S3: juillet 2002 ; References S4: octobre 2002. Abelló P., Villanueva R. & Pili J.M. 1990. Epibiosis in deep-sea A. Depth crab populations as indicator of biological and behavioral Cirripedia Polychaeta Bivalvia Bryozoa characteristics of the host. Journal of the Marine Biological D1 vs D2 0.009 < 0.001 0.022 0.002 Association of the United Kingdom, 12: 687-695. D1 vs D3 < 0.001 < 0.001 0.150 < 0.001 Barnes H. & Bagenal T.B. 1951. Observations on Nephrops D2 vs D3 0.045 0.322 < 0.001 < 0.001 norvegicus (L.) and on an epizoic population of Balanus crenatus Brug. Journal of the Marine Biological Association of the United Kingdom, 30: 369-380. B. Sampling period Bauers R.T. 1981. Grooming behavior and morphology in the Cirripedia Polychaeta Bivalvia Bryozoa decapod crustacean. Journal of Crustacean Biology, 1: 153-173. Becker K. 1996. Epibiont on carapaces of some malacostracans S1 vs S2 < 0.001 0.076 0.943 0.510 from the Gulf of Thailand. Journal of Crustacean Biology, 16: S1 vs S3 < 0.001 0.040 0.417 0.328 92-104. S1 vs S4 < 0.001 < 0.001 0.069 0.972 Biron M., Wade E., Moriyasu M., DeGrâce P., Campbell R. & S2 vs S3 0.187 0.996 0.803 0.992 Hébert M. 2000. Assessment of the 1999 snow crab S2 vs S4 0.447 0.057 0.288 0.340 (Chionoecetes opilio) fishery off eastern Nova Scotia (Areas S3 vs S4 0.965 0.096 0.811 0.207 20 to 24). Department of Fisheries and Oceans. Canadian Stock Assessment Secretariat Research Document, 2000/017. Biron M., Savoie L., Campbell R., Wade E., Moriyasu M. & by the search of a particular range of temperatures (Brêthes DeGrâce P. 2002. Assessment of the 2001 snow crab et al., 1987; Biron et al., 2000; Dionne et al., 2003) and (Chionoecetes opilio) fishery off eastern Nova Scotia (Areas homogeneous muddy substrata (Powles, 1968). Snow crabs 20 to 24). Department of Fisheries and Oceans. Canadian are believed to synchronize their inshore migrations with Stock Assessment Secretariat Research Document, 2002/011. temperature in order to maintain a stable thermal Biron M., Savoie L., Sabean C., Wade E. & Moriyasu M. 2003. environment to sustain their locomotory activities (Lovrich Assessment of the 2002 snow crab (Chionoecetes opilio) et al., 1995). The mobility of the snow crab also confuses fishery off eastern Nova Scotia (Areas 20 to 24). Department the relationship between fouling community and depth. Our of Fisheries and Oceans. Canadian Stock Assessment study showed differences in the fouling communities Secretariat Research Document, 2003/012. between crabs sampled in shallow waters (< 150 m) versus Brêthes J.-C., Coulombe F., Lafleur P.-E. & Bouchard R. 1987. Habitat and spatial distribution of early benthic stages of those sampled in deep waters (> 150 m) of the Sydney the snow crab Chionoecetes opilio O. Fabricius off the north Bight. 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