Mar Biol (2011) 158:31–46 DOI 10.1007/s00227-010-1540-3
ORIGINAL PAPER
Spatiotemporal coupling/decoupling of planktonic larvae and benthic settlement in decapods in the Scottish east coast Maria Pan • Graham J. Pierce • Carey O. Cunningham • Steve J. Hay
Received: 1 December 2009 / Accepted: 28 August 2010 / Published online: 6 October 2010 Ó Springer-Verlag 2010
Abstract Settlement patterns and the relationship between meroplanktonic larvae and settlement in decapods were studied on the Scottish east coast. Artificial settlement substrates (ASS), deployed at two locations (sandy vs. rocky sea substrates), were employed to collect megalopae and newly settled juveniles. Abundance of meroplanktonic larvae was used as an indicator of larval supply. The results showed a clear seasonality in settlement rates, and in some cases, significant differences between sites were detected. Nevertheless, the interference of the ASS with the surrounding habitat limits the study of spatial variability in settlement rates. Significant cross-correlation was found between the abundance of megalopae and juveniles in the collectors and planktonic larval abundance a month earlier. For individual species, this relationship was observed only in Pisidia longicornis. Complexities caused by the great variety of pre- and post-settlement processes, alongside effects of secondary dispersals of early juveniles may
Communicated by P. Kraufvelin. M. Pan (&) C. O. Cunningham S. J. Hay Marine Scotland, Victoria Rd, PO Box 101, Aberdeen AB11 9DB, United Kingdom e-mail:
[email protected] G. J. Pierce Oceanlab, University of Aberdeen, Main Street, AB41 6AA Newburgh, Aberdeenshire, UK G. J. Pierce Instituto Espan˜ol de Oceanografı´a, Centro Oceanogra´fico de Vigo, P.O. Box 1552, 36200 Vigo, Spain
have obscured the relationship between meroplanktonic larvae and juveniles in other species.
Introduction In marine benthic invertebrates with complex life cycles, such as decapod crustaceans, settlement and subsequent recruitment are crucial processes affecting their population dynamic, a central issue in marine ecology studies. The influence of pre- and post-settlement processes in the adult population has been the subject of multiple studies, and attempts have been made to find a relationship between larval supply and recruitment, and the benthic populations. Also, the links between larval supply and settlement are not clearly established. Although in some studies a positive relationship has been found between larval supply and settlement (Gime´nez and Dick 2007), in other cases there is a lack of correlation between the two processes (Loher and Armstrong 2000; Moreira et al. 2007) or limitations in the relationship; Quijo´n and Snelgrove (2005) found a correlation only when later larval stages were considered, and Miron et al. (1995) obtained the best correlation results using data from larval stages close to settlement. These and other studies (Moksnes and Wennhage 2001; Paula et al. 2006) have advised on the multiple biotic (larval developmental stage, behavioural component of larvae and settlers, migration, predation) and abiotic (physical processes affecting larval transport) factors that can affect and obscure the correlation between larval supply and settlement or recruitment. There is a high mortality associated with the early phases of the life cycle, and the likelihood of survival is enhanced by the behaviour of the larvae, selecting the most suitable substrate on which to settle (Ferna´ndez et al. 1993; Palma et al. 1998; Moksnes 2002; van Montfrans et al.
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2003), and being able to delay their metamorphosis into a juvenile until an appropriate settlement habitat is found. Since megalopae or decapodid (the settling stage of decapods) settle preferentially in specific areas, the distribution of early juveniles will not be random. Spatial patterns of settlement are also related to larval transport processes (Wahle 2003). The importance of oceanographic processes, winds, tides, moon cycles and diel cycles in the transport of larvae to settlement grounds has been emphasized in many studies (Queiroga and Blanton 2005; Queiroga et al. 2006, 2007; Peliz et al. 2007). In the present study, we investigated the patterns of decapod settlement in two sites in the north-east Scotland (UK) and the possible coupling with planktonic decapod stages. Artificial settlement substrates (ASS) have commonly been used to study larval supply and the spatiotemporal patterns and rates of decapod larval settlement. The ASS sample passively while immersed and are intended to provide the settlement needs for the new settlers, which attach themselves to the substrate through thigmotactism. In this work, ASS were employed to gather data on decapod settlement patterns. The type of collectors used was different to those found in the literature (e.g. Amaral and Paula 2007) and consisted of plastic spat bags with a mesh rolled up inside, thus creating a complex structure that could be chosen by the potential settlers due to the protection that the collector would provide. These traps were deployed during a 10 month period at two sites representing two different types of habitats: benthic rocky and benthic sandy substrates. To investigate the coupling of early benthic phases of decapods with the meroplanktonic larvae, plankton samples were collected and analysed in order to provide an indicator of larval supply. Since the distribution patterns of early life stages of decapods and other benthic invertebrates with complex life cycles is determined by the behaviour of the settling stage, which selects the substrate, we expect to find differences between the two locations where the collectors were deployed. Complex substrates that can provide shelter from predators are preferred by the settlers (Robinson and Tully 2000b; Pallas et al. 2006). Therefore, our hypothesis is that settlement rates will be higher in the benthic rocky area than at the sandy site. Even though the collector is an artificial substrate, we argue that if settlement rates are naturally higher in a specific area, this will also be reflected in the ASS.
Mar Biol (2011) 158:31–46
Fig. 1). Location 1 (56°59.040 N 02°09.800 W) was the closest to the coast, the seabed substrate was sand and the depth at this point was 22 m. The seabed substrate at location 2 (56°59.640 N 02°07.090 W) was rocky covered by macroalgae and the depth was 37 m. The settlement traps employed consisted of a set of two collectors, placed around a central ring, composed of a black polythene spat bag with a standard bundle of softer fine mesh rolled up inside. The fine mesh ‘‘bundle’’ was expected to offer protection to the early juveniles and may be selected as a settlement substrate by the megalopae. The surface area of each collector was 0.5 m2, and the abundance of the species present in the collectors was expressed as individuals per square metre (ind m-2). Collector sampling was carried out from May 2005 until November 2005 and then started again in February 2006 until June 2006. Every 15 days, the two collectors in each set were removed and substituted with new collectors. Although it was intended to keep the time between sampling days as close to 15 days as possible, on occasions poor weather conditions did not allow this. When retrieved from the sea bed, the individual collectors, colonized by the benthic community, were placed in dark plastic bags and washed clean with freshwater in the laboratory. The samples were preserved: one of the two replicates in 4% borax buffered formaldehyde and the other replicate in 100% ethanol. This was performed to provide samples for future genetic analyses. Zooplankton samples were collected using a bongo net of 40 cm diameter and 200 lm mesh size from the same area where the collectors were deployed (56°57.80 N 02°06.20 W). The net was hauled vertically from 45 m
Materials and methods Sampling Artificial settlement substrates were deployed on the sea bed at two stations near Stonehaven (east coast of Scotland,
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Fig. 1 Map of Stonehaven area, on the east coast of Scotland. Dots 1 and 2 indicate stations where collector arrays were deployed; P indicates where plankton samples were collected. Lines on the inset map are isobaths
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depth at ca. 20 m min-1, and the samples were immediately preserved on board in 4% buffered formaldehyde. Since no flowmeter was fitted to the net, the filtered water volume was calculated based on the net mouth area (0.125 m2) and vertical distance (45 m). These estimates were adjusted assuming 70% filtration efficiency (personal observation). Two plankton samples per month, from January 2005 until June 2006, were analysed and decapod larvae, except infraorder Brachyura, identified to the lowest possible taxonomic level. Sample analysis At the time of their analysis, the collector samples were washed through a 1-mm sieve and then a 250 lm sieve. Many macro organisms from the benthos were present in the samples, although only decapods were extracted and identified to the lowest possible taxonomic level following Hayward et al. (1995) for adults in general, Smaldon (1993) for adult carideans, Ingle (1993) for hermit crab adults and Gonza´lez-Gurriara´n and Mendez (1986) and Ingle (1983) for adult brachyurans. Juveniles were identified following adult keys, megalopae descriptions and when available, papers describing the complete or the juvenile development of the species (e.g. Ingle 1981, 1982; Ingle and Rice 1984). Megalopae and larvae were identified following dos Santos and Gonza´lez-Gordillo (2004), the ICES keys for decapod larvae (Fincham and Williamson 1978; Pike and Williamson 1958, 1972 and Williamson 1957a, b, 1960, 1962, 1967, 1983 and Ingle 1992) and, when available, papers describing the complete larval development. In addition, measurements of megalopae, juveniles and adults were taken in order to facilitate the identification of developmental stages. For Caridea, Paguridae and Galatheidae the carapace length (C.L.: from the base of the eyestalks to the mid-dorsal posterior margin of the carapace) was measured, and for brachyurans and other anomurans the carapace width (C.W.: the greatest width between the lateral extremes of the carapace) was measured. In carideans, the transition from megalopa to juvenile is progressive and this makes it difficult to distinguish these stages. In the appendix, some of the criteria, mainly referring to sizes, used for the identification of stages for the species found in the collectors are shown. This is not a list of identification characters for species but for developmental stages. When morphological features alone were not enough to discern between megalopae, juveniles and adults, sizes were used. The size at maturity was used to differentiate juveniles and adults. When ovigerous females were found in the samples and no information from the literature was available, the size of the smallest ovigerous female was considered as the minimum size for sexual maturity.
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Data analyses Settlement patterns The collectors proved to be very effective in terms of the numbers of decapods found and samples from one sampling event per month were analysed. The samples were chosen based on the temporal distance between samples, trying to keep it as constant as possible i.e. as close to 30 days. An initial data exploration showed a large variation in the abundance data, and a log(N ? 1) transformation was applied (N being the abundance of the species expressed as ind m-2). The non-parametric Analysis of Similarities (ANOSIM) method, using Jaccard’s coefficient as a measure of similarity, was applied to test whether there were differences in the abundance of decapods present in the collectors between both sites. In addition, possible differences in settlement rates between sites and seasons were investigated using generalized linear models (GLM), applying a quasi-Poisson model (i.e. assuming an overdispersed Poisson distribution for the response variable) and using a log link function. Season 1 corresponded to the months March, April and May; Season 2 included the months June, July and August and season 3, September, October and November. The GLMs were applied to total decapods and to juveniles and megalopae separately, and also to those taxa present in the collectors in proportions higher than 5%. These taxa were as follows: Galathea spp., Pisidia longicornis (Linnaeus, 1767), Eualus pusiolus (Krøyer, 1841), Hippolyte spp., Pandalus montagui Leach, 1814 and Family Portunidae. Benthic-pelagic coupling Monthly averages of the total number of decapod larvae in the plankton obtained from the analyses of plankton samples from June to November 2005 and from March to June 2006 were compared with the monthly abundances of megalopae, juveniles and total decapods identified in the collector samples. A possible relationship between both sets of data was explored using the Spearman rank coefficient, a robust correlation function that is applied to ranktransformed data. It was also applied to those species that were both present in the collectors in abundances higher than 5% and were identified in the plankton samples. Those taxa were Pisidia longicornis, Galathea spp., Eualus pusiolus and Hippolyte spp. The analysis was repeated allowing a time lag of 1 or 2 months between plankton and settlement counts. In all analyses, megalopae (settling stage), juveniles and total decapods found in the collectors were analysed
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Mar Biol (2011) 158:31–46
Table 1 Abundances and mean densities of taxa found in collector samples from location 1 Taxon
Location 1 Megalopae N8 of ind.
Relative abundance (%)
ind m-2
Juveniles SD
ind m-2
Adults SD
ind m-2
SD
Anomura Galathea intermedia Galathea spp. Munida spp. Pagurus bernhardus Pagurus spp. Anapagurus spp.
84
2.52
0
0
4.2
8
0
0
161 11
4.83 0.33
4 0
17.9 0
4.05 0
9.1 0
0 0
0 0 0
3
0.09
0.15
0.67
0
0
0
23
0.69
0.2
0.7
0.8
1.61
0.15
0.49
0
0.00
0
0
0
0
0
0
0
0
0.1
0.45
Family Paguridae
19
0.57
0.2
0.89
0.75
1.68
Pisidia longicornis
784
23.53
29.5
72.94
8.75
14.41
11.15
26.23
Caridea Pandalus montagui
276
8.28
1.95
5.74
0.7
1.34
Pandalina brevirostris
1
0.03
0.05
0.22
0
0
0
0
Pandalidae Unidentified
9
0.27
0.4
1.79
0
0
0.05
0.22
14.3
Eualus pusiolus
320
9.60
1.6
5.18
0.1
0.31
Eualus gaimardi
1
0.03
0
0
0.05
0.22
0
0
Eualus occultus
0
0.00
0
0
0
0
0
0
Eualus spp. Unidentified
6
0.18
0.3
1.34
0
0
0
0
1,002 0
30.07 0.00
0.1 0
0.45 0
49.4 0
0.6 0
1.76 0
Caridion gordoni
0
0.00
0
0
0
0
0
0
Pontophilus spinosus
1
0.03
0
0
0
0
0
0
8
0.24
0.15
0.67
0.25
0.64
0
0
Hyas coarctatus
57
1.71
0
0
2.85
4.42
0
0
Macropodia rostrata
33
0.99
0.1
0.45
1.55
3.22
0
0
3
0.09
0
0
0.15
0.67
0
0
Hippolyte spp. Caridion steveni
26.83
83.84 0
Brachyura Ebalia spp.
Macropodia tenuirostris Macropodia spp.
1
0.03
0
0
0.05
0.22
0
0
Family Majidae
11
0.33
0
0
0.55
2.46
0
0
Atelecyclus rotundatus
1
0.03
0.05
0.22
0
0
0
0
Corystes casssivelaunus
81
2.43
0.15
0.67
0
0
0
0
Cancer pagurus
140
4.20
4.15
17.41
2.85
6.42
0
0
Family Portunidae
259
7.77
0.45
1.39
12.5
25.45
0
0
29
0.87
0.65
1.27
0
0
0
0
0
0.00
0
0
0
0
0
0
8
0.24
0.25
1.12
0
0
0
0
Brachyura unidentified Thalassinidea Upogebia spp. Unidentified Decapoda Total
3,332
separately. In the case of plankton data, the low densities of megalopae found in the plankton samples did not allow a comparison between megalopae from the meroplankton and early juveniles in the benthic collectors. All analyses were carried out in the software package Brodgar, version 2.5.4 (http://www.brodgar.com/).
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Results Settlement patterns As expected, the collectors deployed on the seabed were quickly colonized by the benthic community, although only
Mar Biol (2011) 158:31–46
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Table 2 Abundances and mean densities of taxa found in collector samples from location 2 Taxon
Location 2 Megalopae N8 of ind.
Relative abundance (%)
ind m-2
Juveniles SD
ind m-2
Adults SD
ind m-2
SD
Anomura Galathea intermedia
80
1.80
0
0
4.06
8.80
0.39
1.65
1,374 20
30.93 0.45
0 0
0 0
75.39 0.11
194.75 0.47
0.72 0
3.06 0
Pagurus bernhardus
1
0.02
0
0
0
0
0
0
Pagurus spp.
4
0.09
0
0
0.22
0.55
0
0
Anapagurus spp.
8
0.18
0
0
0.22
0.43
0.17
0.71
Galathea spp. Munida spp.
Family Paguridae Pisidia longicornis
21
0.47
1,096
24.67
0 32.50
0 70.09
1.06
1.39
0.11
0.47
26.56
54.26
1.5
2.55
13.06
Caridea Pandalus montagui
2.72
0
0
6.72
0
0
Pandalina brevirostris
0
0
0
0
0
0
0
0
Pandalidae unidentified
3
0.07
0
0
0.17
0.71
0
0
735
16.54
38.78
65.54
Eualus pusiolus Eualus gaimardi Eualus occultus Eualus spp. unidentified Hippolyte spp. Caridion steveni
121
0.33
1.41
1.72
3.44
0
0
0
0
0
0
0
0 0
5
0.11
0
0
0.28
1.18
0
19
0.43
0
0
1.06
2.82
0
0
479 4
10.78 0.09
0 0
0 0
26.33 0.17
45.49 0.51
0.28 0.06
0.67 0.24
Caridion gordoni
6
0.14
0
0
0.17
0.71
0.17
0.51
Pontophilus spinosus
0
0
0
0
0
0
0
0
3
0.07
0
0
0.17
0.51
0
0
0.11
0.47
Brachyura Ebalia spp. Hyas coarctatus
146
3.29
0.17
0.71
7.83
13.73
Macropodia rostrata
6
0.14
0
0
0.33
0.69
0
0
Macropodia tenuirostris
0
0
0
0
0
0
0
0
Macropodia spp.
3
0.07
0
0
0.17
0.51
0
0
Family Majidae
6
0.14
0.33
0.97
0
0
0
0
Atelecyclus rotundatus
0
0
0
0
0
0
0
0
Corystes casssivelaunus
0
0
0
0
0
0
0
0
163
3.67
0.5
1.89
8.56
0
0
Family Portunidae
33
0.74
0.11
0.47
1.72
3.89
0
0
Brachyura unidentified
19
0.43
0.33
0.69
0
0
0
0
1
0.02
0
0
0
0
0
0
87
1.96
0
0
4.83
6.78
0
0
Cancer pagurus
Thalassinidea Upogebia spp.
27.79
Unidentified Decapoda Total
4,443
decapods were identified. All decapod stages were found in the collector samples: zoeae, megalopae, juveniles and adults. The main interest in this study was the megalopae and juveniles, which can indicate settling events during the periods when the collectors remained on the sea bed. In both locations, the great majority of the decapods found
were juveniles, with megalopae being the next most abundant stage. Numbers of adults and zoeae were very low. For the zoea found, 58% were in the last zoeal stage, indicating that the larvae were close to metamorphosis to the megalopa stage. Conversely, another 27% corresponded to the first zoea, suggesting that females had just
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Location1 2000
Megalopae
1600
Ind/m 2
Fig. 2 Mean densities of megalopae and juveniles in the collectors in the two sampling locations. In location 2, the collectors from August were lost at sea (n/d indicates missing data)
Mar Biol (2011) 158:31–46
Juveniles
1200 800 400 0
Jun 05
Jul
Aug
Sep
2000
Oct
Nov
Mar 06
Apr
May
Jun
Location2
Ind/m 2
1600 1200 800 400
n/d
0 Jun 05
Jul
released them. Approximately 50% of the adults present in the samples were Eualus pusiolus or Pisidia longicornis. At least 25 taxa were present in the collector samples analysed. In Tables 1 and 2, the abundances of each taxon for each location are detailed, including those groups where unidentified specimens were aggregated. The most abundant taxon in the sandy location and closest to the coast was Hippolyte spp., followed closely by Pisidia longicornis. In location 2, the most abundant was Galathea spp. followed by P. longicornis. In 2005, there appeared to be two main periods of settlement for both sites (Fig. 2), the first one lasted until June and the other period was through August, September and October. In November, the density of juveniles was lower. In spring of the next year, 2006, some juveniles were present from March, but the first settlement period appeared to start in May. In both locations, the maximum number of juvenile taxa identified per collector was 11: occurring in September and October at location 1 and in September at location 2. The seasonality in locations 1 and 2, of those taxa with relative abundances higher than 5%, is shown in Fig. 3. Galathea spp. was the main contributor to the high density of juveniles recorded in June 2005 in location 2. This species was present at both sites, and the densities appeared to be similar except for June. The highest abundance for most of these taxa occurred in August, September and October although high densities were also recorded in June. ANOSIM applied to the collector data revealed no differences in the abundance of decapods present in the
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Aug
Sep
Oct
Nov
Mar 06
Apr
May
Jun
collectors, between the two sites (Fig. 4). The STRESS obtained when two axes were calculated was 0.02, indicating an excellent configuration, therefore reliable results (Zuur et al. 2007). The P-value obtained in the ANOSIM test using 9,999 permutations and using ‘‘site’’ as blocking variable was 0.108; therefore, the null hypothesis (no differences between sites) could not be rejected. Since the ANOSIM test did not show differences between sites, data from both locations were aggregated in the analyses performed for the study of the relationship between plankton and settlement data. The GLMs applied did not in general show any differences between sites, agreeing with the ANOSIM results, but they showed differences between seasons. Significant differences between sites were detected only for total juveniles, the taxa Galathea spp. and family Portunidae. The numerical output from these models can be found in Table 3. Benthic-pelagic coupling Decapod larvae collected from plankton samples were aggregated into 21 groups (Table 4). Their occurrence in the meroplankton presented two abundance peaks, the first one during spring (March–May) and a secondary peak during the summer, extending into autumn (July–October) (Fig. 5). Comparing the data from the collectors with the results from the analyses of the plankton samples over the same
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Location 1
Location 2 Megalopae
3
log (N+1)
Fig. 3 Taxa present in collector samples in proportions higher than 5%. In location 2, no data were available for August 2005 (indicated by n/d). Data are expressed as the logarithm of ind m-2
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Juveniles
Galathea spp.
Galathea spp.
2
2
1
1
0
0
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
log (N+1)
3
Pisidia longicornis
Pisidia longicornis 3
2
2
1
1
0
0
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
log (N+1)
3
3
Eualus pusiolus
2
1
1
0
0
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
log (N+1)
2
2
1
1
0
0
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
log (N+1)
3
Pandalus montagui
3 2
1
1
0
0
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
log (N+1)
2
2
1
1
0
0
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
period of time (Fig. 5), it can be seen that the two abundance peaks detected in the meroplanktonic larvae (spring and summer-autumn peak) also appeared in the sea bed collectors although with a slight delay. Maximum crosscorrelations between monthly plankton data and monthly
Hippolyte spp.
n/d
Pandalu smontagui
n/d Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
3
Family Portunidae
n/d
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
2
3
Eualus pusiolus
Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06 3
Hippolyte spp.
n/d Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
2
3
n/d Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
Family Portunidae
n/d Jun Jul Aug Sep Oct Nov Mar Apr May Jun 05 06
abundances of megalopae and juveniles (analysed separately), and total decapods in the collectors were found for a time lag 1, i.e. a month delay between plankton and collector data, significant at the 5% level (Table 5). For those species with relative abundances higher than 5% in
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Mar Biol (2011) 158:31–46 2
11F1 8B1
1
6B2 6B1 2F2 4B2 6F2 2F1 4B1 2B2 2B1 5B2 5B1 6F1 SF2 SF1
axis 2
17B1 17B2
OF2
0
8B2 11B2 15F1 8F1
OF1 15B1 OB2
8F2
Discussion
11F2 13F2
Settlement patterns
17F1 OB1 15F2
15B217F2
13B1 13F1
-1
-2
-2
-1
0
1
2
axis 1
Fig. 4 ANOSIM diagram; two axes were calculated. STRESS = 0.0236. The codes indicate the samples (e.g. 2B2 indicates second sampling event, location 1 (B), replicate 2; 11F1 indicates eleventh sampling event, location 2 (F), replicate 1)
the collector samples that were also identified in the plankton: Pisidia longicornis, Galathea spp., Eualus pusiolus and Hippolyte spp., Figs. 6 and 7 show the seasonality of the larval stages in the plankton and of the juveniles in the collectors. Maximum cross-correlations between the monthly larval abundance in the plankton and the monthly abundances of megalopae, juveniles and total abundance in the collectors for each of these taxa were also investigated, but significant cross-correlations, at a time lag 1, were found only for Pisidia longicornis data (Table 5). In 2005, Pisidia longicornis was present at a relatively low abundance in the plankton samples compared with previous years (data not shown). During the plankton sampling in 2006, no larvae were detected in the plankton but settlement in the benthos, reflected by the presence of juveniles in the collectors, did take place. Megalopae of this species, indicating it was close to settle, was recorded only in October in the plankton, while in the collectors megalopae were present from July until November. For this species, the Spearman coefficient showed a correlation between its larval abundance in the plankton and in the collectors with a 1 month delay (time lag 1) (Table 5). Galathea spp. showed relatively high abundances in the meroplankton during 2005, showing the classical two main peaks that can be seen in the plankton. Although no data were available from collectors before June 2005, the presence of juveniles in the ASS appears to follow the same pattern. The information from the plankton samples about Eualus pusiolus and Hippolyte spp. is limited. The low larval densities
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and the lack of information from all zoeal stages (particularly Hippolyte spp, which have six zoeal stages but for which only zoea I and zoea III were identified in plankton samples) complicate the interpretation of the relationship between planktonic larvae and settlers.
The high number of juveniles and megalopae present in the samples indicates that the type of collectors used in this study can be appropriate to study early benthic phases of decapod crustaceans. The collectors were quickly colonized by the benthic community, providing a good estimate of the early juveniles of decapods in the benthos. They also appeared to constitute a good settlement substrate for the megalopae, the settling stage, perhaps due to the protection the collectors offered. The accumulated organic matter and the presence of juveniles in the collectors, perhaps attracted from the surrounding areas, might have enhanced the settlement (Paula et al. 2006). For some species, it has been shown that the presence of conspecifics can attract megalopae to the settlement substrates and accelerate the metamorphosis to juvenile (e.g. Harvey 1996; Gebauer et al. 1998, 1999). In the case of Pisidia longicornis, it is known that it settles preferentially in areas where adults are present (Jensen 1991) and this might explain the relatively high abundances of megalopae of this species in the collectors. Nevertheless, there are also some taxa in which the presence of conspecifics has no effect (Ferna´ndez and Castilla 2000), or a deterrent effect (Ferna´ndez 1999). ASS have been commonly used for over 30 years in order to study larval supply and settlement patterns and rates of decapod crustaceans, and in some studies, this method provided good relative estimates of larval supply and settlement (Moksnes and Wennhage 2001). However, Paula et al. (2006) addressed one important concern never tested before, when using ASS: the possible interference of the collectors, which can enhance or reduce the settlement, with the surrounding habitat. Their results showed that settlement rates obtained from artificial substrates versus the natural surrounding habitat were strongly biased. They recommend using ASS with caution, especially when spatial variability is studied. Therefore, the results from our study regarding differences in settlement rates between sites could be biased. Our initial hypothesis considered that higher settlement rates could be found in the collectors located at the rocky bottom site, but in general, we found no consistent differences between the two locations. As Paula et al.
Mar Biol (2011) 158:31–46 Table 3 GLM results from collector data. The abundances of each taxa include megalopae and juveniles stages
39
Response variable
Explanatory variables
Estimate Total decapods
Total Megalopae
Total Juveniles
Galathea spp.
Eualus pusiolus
Hippolyte spp.
* Statistically significant values (P \ 0.05)
Fam. Portunidae
P-value
0.177
0.111
1.582
0.123
0.648
0.122
5.316
\0.001*
Season (3)
0.741
0.123
6.04
\0.001*
Site (2)
0.129
0.088
1.475
0.15
-0.996
0.471
-2.117
0.042*
Season (2)
Intercept
1.288
0.507
2.542
0.016*
Season (3)
1.760
0.494
3.558
-0.399
0.283
-1.413
0.001* 0.167
Intercept
0.045
0.108
0.413
0.682
Season (2)
0.712
0.117
6.066
\0.001*
Season (3) Site (2)
0.786 0.195
0.118 0.084
6.634 2.328
\0.001* 0.026*
-1.370
0.403
-3.399
0.002*
Season (2)
Intercept
1.293
0.394
3.277
0.002*
Season (3)
0.597
0.439
1.359
0.183
0.795
0.283
2.803
0.008*
-0.933
0.302
-3.089
0.004*
Season (2)
0.747
0.330
2.26
0.03*
Season (3)
1.473
0.307
4.791
\0.001*
Site (2)
0.376
0.202
1.867
0.070
Intercept
-1.710
0.626
Season (2)
Intercept
1.928
0.640
3.014
0.005*
Season (3)
1.799
0.650
2.765
0.009*
Site (2)
0.1915
0.312
0.613
0.544
-1.031
0.438
-2.352
0.02 *
0.395 1.950
0.528 0.451
0.748 4.323
0.460 \0.001*
Intercept Season (2) Season (3)
Pandalus montagui
t-value
Intercept
Site (2) Pisidia longicornis
Std. Error
Season (2)
Site (2)
Site 1: location B; Site 2: location F; Season 1: March, April and May; Season 2: June, July and August; Season 3: September, October and November
Estimated parameters
-2.73
0.01*
Site (2)
-0.252
0.273
-0.925
0.362
Intercept
-1.170
0.501
-2.334
0.02*
Season (2)
1.487
0.524
2.839
0.007*
Season (3)
0.645
0.592
1.089
0.284
Site (2)
-0.332
0.347
-0.955
0.3464
Intercept
-19.887
2767.339
-0.007
0.994
Season (2)
19.702
2767.339
0.007
0.994
Season (3)
20.241
2767.339
0.007
0.994
Site (2)
-0.938
0.320
(2006) suggest, this could be related to the interference of the collectors with the surrounding area and in any case, the settlement rates would not represent the natural dynamics in any of the locations. Nevertheless, differences were seen for total juveniles, Galathea spp. and the family Portunidae. The higher density of juveniles in location 2 could be indirectly related with the substrate type. Decapods prefer substrates with complex 3-dimensional structure for settlement (Ferna´ndez et al. 1993; Ferna´ndez and Castilla 2000; Robinson and
-2.93
0.006*
Tully 2000b; Pallas et al. 2006), which would be more readily available around site 2 (rocky substrate) than around site 1 (sandy substrate). The higher number of juveniles in location 2 could be a consequence of migration and secondary dispersal from nearby areas, where higher settlement rates (compared to sandy areas) might have taken place (Reyns et al. 2006) This can also explain the high density of juveniles, mainly Galathea spp., detected in June 2005 in location 2. These differences between sites could also reflect transport processes influenced by local
123
40
Mar Biol (2011) 158:31–46
Table 4 Abundances and mean densities of taxa found in the plankton samples collected from January 2005 to June 2006
Taxon
Plankton N8 of ind.
Relative abundance (%)
ind m-2
SD
Anomura Galathea spp.
385
25.28
128.73
486.10
Munida sp.
113
7.42
37.78
75.55
Pagurus bernhardus
11
0.72
3.68
6.69
Pagurus pubescens
1
0.07
0.33
1.95
Pagurus spp.
4
0.26
1.34
5.43
Anapagurus spp.
17
1.12
5.68
16.62
Pisidia longicornis
23
1.51
7.69
26.95
1
0.07
0.33
1.95
Eualus pusiolus Hippolyte spp.
26 14
1.71 0.92
8.69 4.68
30.79 18.38
Hippolytidae
68
4.46
22.74
49.99
Crangon crangon
15
0.98
5.02
11.60
Crangon allmanni
2
0.13
0.67
2.72
Pontophilus spinosus
4
0.26
1.34
4.65
Philocheras bispinosus bispinosus
4
0.26
1.34
4.65
Processa canaliculata
2
0.13
0.67
2.72
Pandalina brevirostris
30
1.97
10.03
28.23
Callianassa subterranea
28
1.84
9.36
35.01
Upogebia spp.
19
1.25
6.35
23.78
Caridea Caridion gordoni
Thalassinidea
Nephropidae Nephrops norvegicus Brachyura Unidentified Total
0.13
0.67
3.90
33.62
171.19
246.50
242 1,523
15.89 –
– –
– –
Collectors megalopae 4 Collectors Juveniles 3.5
Planktonic larvae
3
log(N+1)
Fig. 5 Planktonic larvae and megalopae and juveniles from collector samples. N ind m-2. Plankton sampling was carried out continuously from January 2005 to June 2006. Data from collectors are from June to November 2005 and from March to June 2006
2 512
2.5 2 1.5 1 0.5 0 Jan Feb 2005
Mar
Apr
Table 5 Maximum cross-correlations at a time lag 1 Plankton Decapod larvae (total) P. longicornis larvae Collectors (total) 0.78* Collectors Megalopae 0.82*
0.84* 0.91*
Collectors Juveniles
0.74*
0.74*
* indicates significant correlation at the 5% level
123
May
Jun
Jul
Aug
Sep
Oct
Nov
Dec
Jan Feb 2006
Mar
Apr
May
Jun
oceanography and coastal morphology, rather than substrate preferences. Even though the results regarding settlement rates between sites may be biased, the seasonality of the settlement in the area was established. As would be expected, the data presented here indicated a clear seasonality, with significant differences between seasons. From the samples analysed, it appears that settlement might start in the area
Fig. 6 Seasonality of Pisidia longicornis (on left side) and Galathea spp. (on right side) in plankton (Zoea I, Zoea II, Zoea III, Zoea IV and Megalopa plankton) and collector samples (Megalopa collectors and Oct
May Jun
Apr Jun
Jun
Mar Apr
Feb
Jan 06
Dec
Nov
Sep Oct
Aug
May
Juveniles collectors
Apr
Feb Mar
Jan 06
Dec
Nov
Megalopa collectors
May
Mar
Feb
Jan 06
Dec
Nov
Sep
Jun
Jun
Apr May Apr May
Jan 06 Feb
Dec
Nov
Sep Oct
Aug
Jul
May Jun
Apr
Mar
Zoea IV
Mar
Feb
Jan 06
Nov Dec
Oct
Sep
3 2.5 2 1.5 1 0.5 0
Aug
Jul Aug
Jun
May
Apr
Feb Mar
Jan 05
3 2.5 2 1.5 1 0.5 0
Sep Oct
Jul
Jun
May
Mar Apr
Feb Mar
Apr May Jun
Apr May Jun
Dec Jan 06
Nov
Sep Oct
Aug
Jun Jul
Apr May
Mar
Jan 05 Feb
Feb Mar
Zoea II
Feb Mar
Jan 06
Nov Dec
Oct
Aug Sep
Jul
May Jun
Apr
Feb Mar
Jan 05
3 2.5 2 1.5 1 0.5 0
Aug
3 2.5 2 1.5 1 0.5 0 Jul
3 2.5 2 1.5 1 0.5 0
Jul
May Jun
Apr
Mar
3 2.5 2 1.5 1 0.5 0
Jun
May
Apr
Mar
Juveniles Collectors Jan 05
Megalopa Plankton
Feb
Oct Nov Dec Jan 06 Feb Mar Apr May Jun
Zoea II
Jan 05
Jan 06 Feb Mar Apr May Jun
Jul Aug Sep Oct Nov Dec
Zoea I
Feb
Jan 05
Jan 05 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan 06 Feb Mar Apr May Jun
Pisidia longicornis
Feb
Jan 05
Jan 05 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan 06 Feb Mar Apr May Jun
3 2.5 2 1.5 1 0.5 0 Feb Mar Apr May Jun
Jan 05 Feb Mar Apr May Jun Jul Aug Sep
3 2.5 2 1.5 1 0.5 0
Oct Nov Dec Jan 06
Jan 05 Feb Mar Apr May Jun
log(N+1) 3 2.5 2 1.5 1 0.5 0
May Jun Jul Aug Sep
Jan 05 Feb Mar Apr
log(N+1)
log(N+1) 3 2.5 2 1.5 1 0.5 0
log(N+1)
Megalopa Collectors
3 2.5 2 1.5 1 0.5 0
log(N+1)
Mar Biol (2011) 158:31–46 41
Galathea spp.
3 2.5 2 1.5 1 0.5 0
Zoea I
Zoea III
Megalopa Plankton
Juveniles collectors). N ind m-2. Collector data from June to November 2005 and from March to June 2006
123
42
Mar Biol (2011) 158:31–46
May Jun
Mar Apr
Jan 06 Feb
Nov Dec
Sep Oct
Jul Aug
May Jun
Mar Apr
Jan 05 Feb
Apr May Jun
Feb Mar
Nov Dec Jan 06
Sep Oct
Jun Jul Aug
Apr May
Jan 05 Feb Mar
Apr
May Jun
Apr
May Jun
Feb Mar
Jan 06
Nov Dec
Oct
Jul
Aug Sep
May Jun
Apr
Feb Mar
Jan 06
Nov Dec
Oct
Jul
Aug Sep
Apr
May Jun
Juveniles Collectors
3 2.5 2 1.5 1 0.5 0 Feb Mar
Mar Apr Mar Apr
May Jun
Feb Feb
Dec Jan 06 Dec Jan 06
Feb Mar
Jan 05
Jun
Apr May
Feb Mar
Jan 06
Oct Oct
Nov Nov
Sep
Aug
Jun Jul
May
Mar Apr
Feb
Zoea IV
Jan 05
Megalopae Collectors
Jan 05
3 2.5 2 1.5 1 0.5 0
Zoea III
3 2.5 2 1.5 1 0.5 0 Nov Dec
Aug Sep
Jul
Apr
May Jun
Feb Mar
Jan 05
Zoea III
May Jun
Sep Oct
Jun Jul
May
Mar Apr
Feb
Jan 05 3 2.5 2 1.5 1 0.5 0
Aug
Zoea VI
3 2.5 2 1.5 1 0.5 0
3 2.5 2
May Jun
Apr
Feb Mar
Jan 06
Nov Dec
Oct
Aug Sep
Jul
Apr
May Jun
Jan 05
Megalopae collectors
Juveniles collectors
Jun
May
Apr
Mar
Feb
Dec
Jan 06
Nov
Oct
Sep
Aug
Jul
Jun
Apr
May
Mar
Jan 05
1.5 1 0.5 0
Fig. 7 Seasonality of Eualus pusiolus (on left side) and Hippolyte spp. (on right side) in plankton and collector samples. N ind m-2. The lack of graphs for some of the zoeal stages indicates that no larvae in that zoeal stage were found e.g. for E. pusiolus no larvae in zoea V or
123
3 2.5 2 1.5 1 0.5 0
May Jun
Apr
Feb Mar
Jan 06
Nov Dec
Aug Sep
Jun Jul
May
Mar Apr
Feb
Jan 05 3 2.5 2 1.5 1 0.5 0
Oct
Zoea II
3 2.5 2 1.5 1 0.5 0
Zoea I
3 2.5 2 1.5 1 0.5 0
Jun
Apr May
Mar
Jan 06 Feb
Oct
Jul
Aug Sep
Apr
May Jun
Feb Mar
Jan 05
Nov Dec
Zoea I
Feb Mar
log(N+1) log(N+1) log(N+1) log(N+1) log(N+1) log(N+1)
Hippolyte spp.
3 2.5 2 1.5 1 0.5 0
Feb
log(N+1)
Eualus pusiolus
megalopae were found in the plankton. For Hippolyte spp., zoea II and C zoea IV were not present. Collector data from June to November 2005 and from March to June 2006
Mar Biol (2011) 158:31–46
in March, with very low densities, and finishes around November. The main settlement period took place between August and October but a secondary settlement event might happen earlier in the year, in May and June. Similar to our observations, Robinson and Tully (2000a) studying the decapod benthic community in south-east Ireland, observed the start of the settlement season in May–June and an increase in densities of juveniles in the benthos until late September. The presence of zoeal stages in the collectors was unexpected, but it must be noted that nearly 60% of the zoeae in the collectors samples were the last zoeal stage, close to the megalopae stage, and these larvae might start to increase contact with the benthos, exploring the available substrates. On the other hand, decapod larvae perform diel vertical migrations as a mechanism to control their horizontal transport (Lindley et al. 1994; dos Santos et al. 2008), and during the day, they maintain vertical position in the deeper layers. The collectors, which were always recovered during the morning, might have simply trapped these zoeae located in deep layers of the water column at the moment of lifting. Plankton-benthic coupling The Spearman coefficient showed maximum cross-correlations between plankton and collector data (megalopae plus juveniles, only megalopae and only juveniles) when a time lag of 1 month was applied. The same analysis was performed for the taxa Pisidia longicornis, Galathea spp., Eualus pusiolus and Hippolyte spp., species with high relative abundances in the collectors. Except for P. longicornis, the larval stages in the plankton were not apparently correlated with the megalopae and juveniles of these taxa present in the collectors. The use of plankton data to estimate larval supply has limitations since most of the planktonic larvae captured are not competent to settle (Moksnes and Wennhage 2001) and before that moment, they will be subject to pre-settlement processes that will affect their survival. Even in the case of megalopae, these do not settle immediately and this delay, along with possible predation, would affect the coupling between larval supply and settlement (Moreira et al. 2007). Nevertheless, we observed two cases where significant cross-correlations were detected, P. longicornis and the total decapods data set. In the case of P. longicornis, pre-settlement factors would have less time to affect the relationship between larvae and juveniles, since this species has only two zoeal stages followed by a megalopa before metamorphosis into a juvenile. In the case of the positive correlation detected between plankton and collector data for total decapods, this might be an artefact of the high proportion of
43
P. longicornis in the collectors. For species with short larval development, the use of plankton data as an indicator of larval supply might be an option. The correlation between the meroplanktonic larvae and the juveniles in the collectors was weaker than the correlation between plankton and megalopae, probably due to the effect of post-settlement processes, on megalopae or early juvenile survival, that start to act after settlement, obscuring the relationship between meroplanktonic larvae and juveniles. The Stonehaven area where the sampling took place is considered a potentially good nursery and settlement ground for several important commercial species of fish: cod (Gadus morhua Linnaeus, 1758), haddock (Melanogrammus aeglefinus (Linnaeus, 1758)) and whiting (Merlangius merlangus (Linnaeus, 1758)) (Demain 2008). Decapod larvae and juveniles are an important part of their diet in their juvenile stages, reaching up to 40% of their dietary composition. Data obtained by Demain (2008) showed that 2005 was a strong year-class for whiting, which predate on decapod crustaceans. Among decapods, Pisidia longicornis were an important diet component. During 2005, this species showed a considerable decrease in abundance in the plankton with respect to previous years although no differences in the recorded environmental variables were found (data not shown). It could be hypothesized that one of the reasons for this reduction in their larval abundance could be related with the prey–predator relationship, so high pressure from predators like whiting could reduce the abundance of P. longicornis. This study has successfully determined the major species present in the region and their general seasonal pattern of occurrence and settlement. This is the first time such information has been obtained in Scottish waters. Future studies will also need more extensive observations of environmental factors that affect the observed rates of development and settlement. Particularly important will be broader data and models of the hydrodynamics of advection and larval transport processes. Acknowledgments The authors would like to thank John Dunn and the Temora crew for their help during collectors and plankton sampling. This work has been funded by a PhD grant to Pan M., provided by FRS Marine Laboratory Aberdeen, now Scottish Government, Marine Scotland-Science, Marine Laboratory, Aberdeen. G.J. Pierce was supported through the EU-funded ANIMATE project (MEXCCT-2006-042337).
Appendix See Table 6.
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Mar Biol (2011) 158:31–46
Table 6 Taxa present in the collectors with some of the characters and sizes employed for the diagnosis of their developmental stages Taxon
Megalopa
Juvenile
Adult/Sexual maturity
Ovigerous females (own data)
Galathea intermedia
C.L.: 1.6–1.8 mm (C&A)
C.L.: 1.8 mm to 4.5 mm (own data)
[4.5 mm (own data)
C.L.: 5.5 mm; 6.9 mm; 4.4 mm
Galathea spp.
C.L.: G. rostrata 1.7 mm (G)
Munida spp. Pagurus berhnardus
Pleopods present. T.L.: No pleopods present, No pleopods present, except in 4.2 mm (ICES) except in females which females which maintain left maintain left pleopods to pleopods to carry the eggs carry the eggs
Pagurus spp.
Pleopods present. T.L.: No pleopods present, No pleopods present, except in P. pubescens: except in females which females which maintain left 3.1 mm; P. prideaux: maintain left pleopods to pleopods to carry the eggs. 4.3 mm (ICES) carry the eggs C.L.: 1.2 mm (Pallas). High range size among species
Anapagurus spp.
Pleopods present. T.L.: No pleopods present, No pleopods present, except in A. laevis 3.6 mm; A. except in females which females which maintain left hyndmanni 2.7 mm; maintain left pleopods to pleopods to carry the eggs. A. chiroacanthus carry the eggs C.L.: 1.2 mm (Pallas) 2.3 mm (ICES)
Fam. Paguridae
Pleopods present
No pleopods present, C.L.: 1.2 mm (Pallas) except in females which maintain left pleopods to carry the eggs
Pisidia longicornis
3 pairs of pleopods
No pleopods present
Pandalus montagui
Exopods on pereiopods No exopod buds. Fewer No exopod buds and present but reduced; segments on P2 right than segmentation on P2 as pleopods fully setose in adults described in the literature. T.L.: and functional. T.L.: usually \ 100 mm (S); 10 mm (M) 40–50 mm (Marlin)
C.L.: 1.5 mm; 1.6 mm; 2.1 mm
No pleopods present. Abdomen C.W.: 5.1 mm; 4 mm; completely folded. Carapace 3.6 mm; 4.7 mm; more calcified. C.W.: 2.8 mm 5.1 mm; 3.2 mm; (Pallas); 3 mm (Marlin); 3 mm 3.8 mm; 4.1 mm; (R&T); 3.2 mm (own data) 3.7 mm; 5.2 mm; 5.2 mm
Pandalina brevirostris (1) Eualus pusiolus
Thoracic exopods No exopods present. reduced but present. Epipods present. P2 Pleopods fully setose carpus usually with six TL.: 4.7–4.8 mm segments (ICES)
P2 carpus with the normal seven T.L.: 13.5 mm; segments. T.L.: 13.5 mm 16.5 mm; 15.5 mm; (own data) 15.3 mm; 15.7 mm; 18.2 mm; 17 mm; 15 mm; 17.9 mm; 16 mm; 16.4 mm; 18.1 mm
Eualus gaimardi (1)
No exopods present. Thoracic exopods Epipods present. P2 reduced but present; pleopods fully setose. carpus usually with six T.L.: 5.4 mm (P&W) segments
P2 carpus with the normal seven segments
Eualus occultus (2)
Thoracic exopods reduced but present; pleopods fully setose.
Hippolyte spp.
Thoracic exopods reduced but present. T.L. 4.7–5.7(M).Exopod buds
Caridion steveni (2)
T.L.: 7.7 mm (M)
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Mar Biol (2011) 158:31–46
45
Table 6 continued Taxon
Megalopa
Caridion gordoni (2)
T.L.: 11–13 mm (ICES)
Juvenile
Adult/Sexual maturity
Ovigerous females (own data)
T.L.: 18 mm (own data)
T.L.: 19.7 mm; 18 mm
Pontophilus spinosus (1) Upogebia sp. (2)
C.L.: U. Deltaura 1.4 mm (M); U. stellata 1.5 mm (M)
Ebalia spp.
C.L.: 1.04–1.28 mm (M)
Hyas coarctatus
C.L.: 2–2.1 mm (M)
Macropodia rostrata
C.L.: 1.2–1.3 mm (M)
Macropodia tenuirostrisi (1)
C.L.: 1.4–1.5 mm (M)
Family Majidae
Highly variable among species
Atelecyclus rotundatus (1)
C.L.: 3.2 –4 mm (M) (H&I)
Corystes casssivelaunus (1) C.L.: 4.2–4.6 mm (M) Cancer pagurus C.L.: 2.9–3.3 mm (M) Necora puber
C.L.: 1.8 mm (M)
‘‘ovigerous females (own data)’’ refers to those ovigerous females that appeared in the collector samples. C.L. carapace length, C.W. carapace width, T.L. total length, P2 second pereiopod, (1): only present in location 1; (2): only present in location 2; (C&A): Christiansen and Anger 1990; (G): Gore 1978; (H&I): Hong and Ingle 1987; (ICES): ICES keys for decapod larvae (Pike and Williamson 1958; Williamson 1957b); (M): Martin 2001; (Pallas): Pallas et al. 2006; (P&W): Pike and Williamson 1961; (R&T): Robinson and Tully 2000a; (S): Smaldon 1993; (Marlin): Marine Information Network for Britain and Ireland http://www.marlin.ac.uk/
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