- Email: [email protected]
Demersal fish and habitat associations from visual surveys on the central California shelf
Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Demersal fish and habitat associations from visual surveys on the central California shelf Thomas E. Laidig*, Diana L. Watters, Mary M. Yoklavich Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, 110 Shaffer Road, Santa Cruz, CA 95060, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 August 2008 Accepted 12 May 2009 Available online 20 May 2009
In 2004, we surveyed demersal fishes and habitats on the continental shelf off central California (65–110 m depth) using the occupied submersible Delta. Our objectives were to estimate the relative abundance of habitats and to examine demersal fish species composition, diversity, density, and sizes relative to these habitats. A total of 112 transects were completed covering 32 km of seafloor. A higher density of fishes was estimated in boulder and cobble habitats than in mud and brachiopod beds. More than 80% of the fishes were small, measuring 20 cm or less in total length. Species with small maximum size (primarily pygmy rockfish, Sebastes wilsoni, and blackeye gobies, Rhinogobiops nicholsii) accounted for nearly half (49%) of the total number of 12,441 fishes. Most fishes were immature, with only 4 of 20 harvested species having more than 50% of the individuals larger than the size at first maturity. Our study area on the continental shelf may be an ontogenetic transition zone for immature fishes before they move to their adult habitat on the slope. Alternatively, historical fishing pressure may have contributed to the lack of large, mature fishes in the survey area. Understanding the importance of these habitats to fishes at various life stages will improve our ability to assess these deepwater fish stocks and effectively manage these living resources on an ecosystem basis. Published by Elsevier Ltd.
Keywords: demersal fishes continental shelf Delta submersible habitat habitat selection community structure
1. Introduction Fish habitat requirements are fundamental to sound fisheries management, particularly in establishing and monitoring effective protected areas. However, many demersal shelf species live at depths that are difficult to study (e.g., >30 m), thereby limiting our understanding of these fishes and their associated habitats. Populations of several demersal species have been declining for years in the northeast Pacific and North Atlantic (Parker et al., 2000; Christensen et al., 2003). Understanding the habitat associations for these species is an important component to developing successful rebuilding plans. Researchers have used quantitative survey methods to gather some information on demersal fishes and their habitats along the West Coast of North America. Much of this work has been conducted from an occupied submersible on offshore banks and in submarine canyons deeper than 100 m (Pearcy et al., 1989; Stein et al., 1992; Yoklavich et al., 2000; Love et al., 2009). Other fish habitat studies have been conducted using SCUBA in waters shallower than 30 m (DeMartini and Roberts, 1990; Carr, 1991; Paddock
* Corresponding author. E-mail address: [email protected] (T.E. Laidig). 0272-7714/$ – see front matter Published by Elsevier Ltd. doi:10.1016/j.ecss.2009.05.008
and Estes, 2000; Laidig et al., 2007). Only a few surveys of fish– habitat associations have been conducted at intermediate depths (30–100 m) on the continental shelf (Yoklavich et al., 2002; Anderson and Yoklavich, 2007; Love and Schroeder, 2007). In this paper, we report on surveys of demersal fishes and habitats at these intermediate depths on the continental shelf off central California using the occupied submersible Delta. This area has been fished since the late 1800s and was closed to most bottom fishing in 2002 (PFMC, 2003), providing an opportunity to develop an early post-fishing baseline. Our objectives were to estimate the relative abundance of habitats and to examine demersal fish species and size composition, diversity, and density relative to these habitats. 2. Methods 2.1. Study site Surveys were conducted on the continental shelf north of Monterey Bay approximately 11 km southwest of Davenport, California (Fig. 1). The study area was 18 km long and 3 km wide (36 520 to 37 020 N; 122110 to 122190 W), and ranged in depth from 65 to 110 m. Much of the sea floor in the study area consisted of soft mud. We focused our surveys in areas of likely habitats of
630
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Fig. 1. Map of the study area off central California. The submersible transects are displayed as colored lines, with each color representing one of the four primary habitats (boulder, cobble, mud, and brachiopod). The dark green Purisima mudstone formation represents the interpreted hard substratum (from Eittreim et al., 2002). Inset: An example of the distribution of different habitat types along a segment of a submersible transect.
Pacific rockfishes (Sebastes spp.) (i.e., hard substratum is dark green in Fig. 1), and locations of previous research longline surveys conducted from 2001to 2004 (D. Pearson, NMFS, Santa Cruz, CA, pers. comm.). 2.2. Fish and habitat surveys Surveys were conducted from 23 August to 4 September 2004 between 07:00 and 17:30 h using the Delta, a 4.6 m-long
submersible that accommodates one scientific observer and one pilot. Survey dates were selected based on the availability of the submersible and consistently calm sea state to maximize survey effort. Three experienced observers collected all data. Up to six 10-min transects were completed during each dive. The direction and location of each transect were guided by scientists monitoring the submersible’s position and communicating with the pilot from the surface support vessel R/V Velero IV. Between each transect, the submersible would run for at least 5 min to a new sampling area
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
determined by the scientist on the Velero IV. The Delta’s position was continuously recorded using WinFrog navigation software and the ORE Trackpoint Ultra Short Base Line system. Navigation data were subsequently edited for outliers and interpolated to onesecond intervals. Transects were later plotted and measured using ArcMap 9.0 GIS software. The submersible traveled at an average speed of 0.9 knots (dependent on the bottom topography), approximately 1 m above the bottom. Three video cameras documented benthic fauna during each dive. One external color camera was mounted above the middle view port on the starboard side of the submersible and recorded habitats and organisms up to approximately 1.5 m above the seafloor. A low-light, black-and-white external camera was aimed forward to view upcoming fishes and terrain. The third camera was located inside the submersible and pointed downward so as to document fauna from the lowest view port on the starboard side. This camera was used to record fishes closest to the submersible along the transect’s inside edge. The scientific observer conducted belt–transect surveys through the middle view port, orally recording onto the three videotapes all fishes observed within two meters of the submersible. The 2-m width of the transect was verified using a hand-held sonar gun. Fishes were identified to the lowest possible taxon and counted. Total length of fishes was estimated using the aide of two parallel lasers mounted 20 cm apart on either side of the middle view port camera as a reference scale. The video footage for each transect was later reviewed and observations confirmed. From this review and the audio-recordings, data were transcribed into a database. Bottom habitat was characterized from the videotapes, using the geological habitat classification system of Greene et al. (1999). Habitat comprised four main substrata: boulder (>25 cm wide), cobble (<25 cm wide), mud, and brachiopod beds, Laqueus californianus. If a substratum covered >50% of the seafloor it was considered the primary habitat. Changes in habitat classification were noted only if they persisted for longer than 3 s on the video transect (the time for an image to move completely across the video monitor, about 1.4 m substrate length). Anderson and Yoklavich (2007) determined that very little information (related to fish–habitat associations) was lost by eliminating these small-scale patches of habitat. Brachiopods occurred individually, in small groups, and in large aggregations (numbering thousands of individuals) attached to hard substrata (e.g., cobbles, boulders, and other brachiopods), which were often covered by a thin layer of mud. We only considered the large, bed-forming aggregations (Fig. 2) covering >50% of the seafloor as a primary habitat in this study.
2.3. Data analysis Those species comprising 5% or more of fishes counted on any given transect were used in statistical analyses. Using this criterion, species that were rare overall but important in the assemblage of specific transects were included in the analysis. Additionally, we noted those species that commonly are recreationally and commercially harvested at this location. A Durbin–Watson statistic was used to test for independence of fish densities between the transects. We examined species associations with habitats by calculating a habitat selectivity index. Because habitat types were not equally abundant, we standardized habitat use to habitat availability by subtracting proportional occurrence of each habitat type from the proportional abundance of each species on that habitat (Anderson and Yoklavich, 2007). We used a chi-square goodness of fit test to determine if species were randomly distributed among habitats.
631
Fig. 2. A large aggregation of brachiopods (Laqueus californianus) off Davenport, CA, in 100 m depth. A small (15 cm total length) greenspotted rockfish (Sebastes chlorostictus) is in the background.
Size distribution was examined for each species by pooling lengths in 5-cm bins. Length at first maturity was established using published data (Phillips, 1964; Hart, 1973; Rothrock, 1973; Echeverria, 1987; Love, 1996; Love et al., 2002; Fishbase, 2007). We chose length at first maturity as a more conservative indicator than length at 50% maturity. No species groups were used due to differences in length at first maturity within these groups. A matrix of species densities (number m2) by transect was constructed for multivariate analysis of species assemblages. Densities were fourth-root transformed to down-weight highly abundant species and to allow the full spectrum of species to contribute to the analysis. Multivariate analyses were performed using PRIMER 6 software (Clarke and Gorley, 2006) to describe associations among fish species and habitat types. Similarities in species densities were calculated for every pair of transects using the Bray-Curtis coefficient (Bray and Curtis, 1957). The resulting similarity matrix was used in a hierarchal cluster analysis (Cormack, 1971) (group–average linking). Similarity profile (SIMPROF) permutation tests were incorporated into the cluster analysis (Clarke and Gorley, 2006) to test each node of the dendrogram for statistically significant groups. Significant groups (p < 5%) were analyzed with a similarity percentage routine (SIMPER) to identify the species that characterized those groups. The SIMPER routine calculated the average similarity between all pairs of transects within each group and determined the contribution that species made to that similarity in two ways: (1) measuring the consistency with which a species contributed (average similarity between transects/standard deviation; high value ¼ consistent presence of a species); and (2) the
Table 1 Mean area and fish density (with standard error in parentheses) for each primary habitat type. Habitat type
Mud Boulder Brachiopod Cobble
Mean area
Mean fish density
(m2)
(#/m2)
151 94 23 18
0.15 (0.03) 0.24 (0.05) 0.02 (0.005) 0.10 (0.03)
(10) (8) (5) (3)
632
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Table 2 Total number, total relative abundance (%), highest percent on any single transect (% highest), and mean total length and standard error (SE) of fish taxa observed from the Delta submersible, summer 2004. Names in bold signify that they were at least 5% of the total fish abundance on any given transect. Common name
Pygmy rockfish Blackeye goby Rosy rockfish Greenspotted rockfish Yellowtail rockfish Greenstriped rockfish Sebastomus YOY rockfish Sanddab spp. Unidentified flatfish Squarespot rockfish Starry rockfish Lingcod Unidentified poacher Pink seaperch Canary rockfish Halfbanded rockfish English sole Bocaccio Northern ronquil Vermilion rockfish Unidentified rockfish Shortspine combfish Copper rockfish Kelp greenling Flag rockfish Unidentified sculpin Rock sole Widow rockfish Speckled rockfish Brown rockfish Slender sole Petrale sole Rosethorn rockfish Calico rockfish Unidentified sculpin Spotfin sculpin Blue rockfish Dover sole Stripetail rockfish Unidentified hagfish Unidentified skate Painted greenling Rex sole Yelloweye rockfish Longspine combfish Threadfin sculpin Cowcod Longnose skate Spotted cusk-eel Unidentified combfish Big skate Greenblotched rockfish Plainfin midshipman Ratfish Starry skate Unidentified prickleback California halibut Northern anchovy Redbanded rockfish Unidentified salmon Wolfeel
Scientific name
Sebastes wilsoni Rhinogobiops nicholsii Sebastes rosaceus Sebastes chlorostictus Sebastes flavidus Sebastes elongatus Sebastomus Sebastes spp. (YOY) Citharichthys spp. Pleuronectidae Sebastes hopkinsi Sebastes constellatus Ophiodon elongatus Agonidae Zalembius rosaceus Sebastes pinniger Sebastes semicinctus Pleuronectes vetulus Sebastes paucispinis Ronquilus jordani Sebastes miniatus Sebastes spp. Zaniolepis frenata Sebastes caurinus Hexagrammos decagrammus Sebastes rubrivinctus Cottidae Lepidopsetta bilineata Sebastes entomelas Sebastes ovalis Sebastes auriculatus Lyopsetta exilis Eopsetta jordani Sebastes helvomaculatus Sebastes dallii Icelinus spp. Icelinus tenuis Sebastres mystinus Microstomus pacificus Sebastes saxicola Myxinidae Rajidae Oxylebius pictus Errex zachirus Sebastes ruberrimus Zaniolepis latipinnis Icelinus filamentosus Sebastes levis Raja rhina Chilara taylori Zaniolepis spp. Raja binoculata Sebastes rosenblatti Porichthys notatus Hydrolagus colliei Raja stellulata Stichaeidae Paralichthys californicus Engraulis mordax Sebastes babcocki Oncorhynchus spp. Anarrhichthys ocellatus
Total number
2897 2191 1130 809 730 627 509 466 393 366 344 240 204 182 157 145 131 103 97 96 82 77 67 44 43 37 28 27 25 19 18 15 12 12 11 11 9 8 8 8 7 7 6 6 6 5 4 3 3 3 3 2 2 2 2 2 2 1 1 1 1 1 12448
percent contribution of a species to the overall similarity of the group. We used non-metric multidimensional scaling (MDS) to further examine species assemblages among transects. A stress value indicates the degree of difficulty in constraining the relationships
% Total
23.4 17.7 9.1 6.5 5.9 5.1 4.1 3.8 3.2 3.0 2.8 1.9 1.6 1.3 1.3 1.2 1.0 0.7 0.7 0.7 0.6 0.6 0.5 0.4 0.3 0.3 0.2 0.2 0.2 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 100.0
% Highest
79.5 55.0 31.1 41.8 25.8 5.7 28.1 44.4 84.8 40.0 7.9 27.4 12.9 47.7 15.4 22.0 54.0 29.0 6.7 10.9 9.1 1.8 10.6 3.9 5.8 3.6 6.8 5.7 16.4 3.3 4.4 3.8 5.1 3.4 8.6 7.0 2.9 3.9 5.6 5.9 11.1 3.7 1.1 5.0 1.0 2.8 7.0 1.8 2.9 2.0 2.9 1.9 1.4 3.8 1.1 1.4 1.4 3.8 4.7 1.7 1.4 0.5
Mean length
Length
(cm)
(SE)
9.1 7.3 16.5 19.2 27.9 12.9 10.2 5 11.0 12.7 15.1 20.0 36.2 11.4 12.8 32.2 14.5 20.0 42.5 10.4 33.9 13.8 16.8 34.3 28.3 21.4 8.4 17.5 26.8 25.6 25.9 13.7 16.3 19.5 13.6 9.5 10.6 25 16.9 10.6 17.5 37 11.7 16.7 32.5 17 7.5 46.7 40 10 13.3 35 32.5 12.5 50 42.5 10 40 10 20 50 20
0.0 0.1 0.1 0.3 0.2 0.2 0.3 0.01 0.3 0.3 0.2 0.4 0.8 0.3 0.2 0.8 0.3 0.5 1 0.3 0.7 0.8 0.5 0.7 0.5 1 0.7 1 1.1 0.9 1.4 0.9 2.3 1.3 0.9 1.3 1 0 1.3 1.8 2.5 6.6 1.1 1.7 3.1 2.5 2.5 6 0 0 3.3 5 2.5 2.5 N/A 2.5 N/A N/A N/A N/A N/A N/A
into low dimensional space (i.e., stress values <0.1 indicate relatively good ordination, whereas values >0.3 indicate relatively poor ordination). PRIMER global BEST match-permutation test was used to evaluate a null hypothesis of no agreement in multivariate patterns among species and habitats from the same transects. This
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
633
Table 3 Length at first maturity (total length, cm) for 22 species comprising at least 5% of the total abundance on any given transect. Number and percent of fishes less than or equal to length at first maturity are indicated. Names in bold signify fish that are harvested. Common name
Length at 1st maturity
Total fish measured
Number less than first maturity
% less than first maturity
Reference
Calico rockfish Bocaccio Shortspine combfish Squarespot rockfish Halfbanded rockfish Canary rockfish Kelp greenling Vermilion rockfish Blackeye goby Widow rockfish Rosy rockfish Greenstriped rockfish Lingcod Greenspotted rockfish Stripetail rockfish Yellowtail rockfish Starry rockfish English sole Rock sole Dover sole Petrale sole Rex sole
7 32 15 13 10 27 29 31 5 26 16 15 40 25 15 30 25 25 28 30 38 17
9 96 67 341 131 105 38 81 2189 25 1120 626 196 798 8 723 235 103 26 8 12 6
0 6 58 66 28 34 16 35 1176 14 652 458 147 686 7 640 209 99 25 8 12 6
0 6 9 19 21 32 42 43 54 56 58 73 75 86 88 89 89 96 96 100 100 100
6 4, 6 7 4, 6 6 2, 1, 4 3 4, 6 5 4, 6 4, 6 4, 6 5 4, 6 4, 6 4, 6 4, 6 2 2 2, 5 2, 5 5
References: 1, Phillips, 1964; 2, Hart, 1973; 3, Rothrock, 1973; 4, Echeverria, 1987; 5, Love, 1996; 6, Love et al., 2002; 7, Fishbase, 2007.
test finds the best match among the species assemblage patterns and habitat types associated with transects. 3. Results A total of 112 transects were completed during 28 dives covering 32 km of seafloor in 12 days (Fig. 1). The Durbin–Watson statistic was 1.9, demonstrating no statistical dependence among the transects. The dominant habitats were mud and boulder, with a mean of 151 and 94 m2 transect1 and representing 53% and 32% of available habitats respectively (Table 1). Brachiopod beds and cobble were much less abundant, representing on average 41 m2 transect1 (14%) of the surveyed seafloor. Mean fish density was highest in boulder habitat (0.24 fish m2), and lowest in brachiopod habitat (0.02 fish m2) (Table 1; Appendix A). A total of 12,448 fishes were observed during this study, with 10,396 (84%) identified to species. Fishes were identified to 62 taxa, including 49 species, 7 genera and subgenera, and 6 families (Table 2). Thirty-four of these taxa comprised at least 5% of the total number of fishes observed on a given transect and therefore were included in further analyses. Small fishes dominated the survey, with 85% measuring 20 cm or less in total length (Table 2). Pygmy rockfish, Sebastes wilsoni (n ¼ 2897), and blackeye goby, Rhinogobiops nicholsii (n ¼ 2191), both non-harvested and small-bodied species, were the two most abundant species. These two small species accounted for 41% of all fishes in this study. Rockfishes accounted for 67% of all fishes and 74% of all fishes 20 cm or less in total length. Of the 22 species for which maturity data have been published, greater than 50% of individuals of 14 species were smaller than or equal to the length at first maturity (Table 3; Fig. 3). Twenty species were classified as harvested, and only 4 of these comprised mostly mature individuals (greater than 50%): kelp greenling (Hexagrammos decagrammus), bocaccio (Sebastes paucispinis), and canary (Sebastes pinniger) and vermilion (Sebastes miniatus) rockfishes. Twenty-eight of the 34 species groups had a non-random habitat-use pattern (chi-square statistic p < 0.05; Table 4). The 6 species that were randomly distributed (indicated with an asterisk on Table 4) all had low sample sizes (n ¼ 4–28 individuals). Most
species were positively associated with boulder habitat, while some species were positively associated with mud (e.g., flatfishes (Pleuronectidae), greenstriped rockfish (Sebastes elongatus), pink surfperch (Zalembius rosaceus), and poachers (Agonidae)). The lowest numbers of species were positively associated with brachiopod beds and cobble. Greenspotted rockfish (Sebastes chlorostictus) were positively associated with all but mud habitats and did not have greater selectivity for any one habitat. Within the cluster analysis, SIMPROF tests identified 17 groups of transects (a–q) that were significant (p < 5%). The MDS ordination, (stress value ¼ 0.15), produced comparable groups to that of the SIMPROF analysis. Two groups (a and h) consisted of single transects and could not be analyzed by SIMPER. One of these was dominated by high numbers of unidentified sanddabs (Citharichthys spp.) (82%), and the other by greenspotted, rosy (Sebastes rosaceus), and squarespot (Sebastes hopkinsi) rockfishes, and blackeye gobies. Within the 15 groups that were analyzed with SIMPER, average percent similarity of transects ranged from 60% to 87% (Table 5). These groups were typified by five to ten species that cumulatively contributed 90% of total similarity, and were consistently abundant throughout the transects in their group, as indicated by mean similarity/SD values. There was a high degree of overlap in species among some groups, with many species occurring in multiple groups. Fish assemblages that occurred over boulder habitat were of two general types (Table 5): one in which pygmy rockfish dominated (19–22% contribution), and the other without pygmy rockfish. Rosy, yellowtail (Sebastes flavidus), and starry rockfishes (Sebastes constellatus), the subgenus Sebastomus, and blackeye gobies were consistent members of both types of assemblage on boulder habitat. Flatfishes, poachers, sanddabs, and greenstriped rockfishes characterized the species assemblages that occurred on muddominated habitat. Assemblages of greenstriped and greenspotted rockfishes, lingcod (Ophiodon elongatus), and blackeye gobies were associated with brachiopod beds. Cobble was dominant in only one instance, preventing an analysis of the assemblages occurring on this habitat. The null hypothesis of no agreement in multivariate pattern between the species and habitat similarity matrices was rejected by the global BEST match test (r ¼ 0.67, p ¼ 0.1%). The
634
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
0.25
Greenspotted rockfish n=798
0.30
Vermilion rockfish n=81
0.25
0.20
0.20 0.15 0.15 0.10 0.10 0.05
0.00
0.05
5
10
15
20
25
30
0.35
35
40
Starry rockfish n=235
0.30
0.00
0.35 0.30
0.25
0.25
0.20
0.20
0.15
0.15
0.10
0.10
0.05
0.05
0.00
5
10
15
20
25
30
0.30 Lingcod n=196
0.25
0.00 0.50 0.45
15
20
25
30
35
40
45
Bocaccio n=96
20
25
30
35
40
45
50
55
60
65
70
Canary rockfish n=105
0.40 0.35
0.20
0.30 0.15
0.25 0.20
0.10
0.15 0.10
0.05
0.05 0.00
20 25 30 35 40 45 50 55 60 65 70 75 80
Size class (cm)
0.00
10
15
20
25
30
35
40
45
Size class (cm)
Fig. 3. Size distribution (total length, cm) of six representative species (species that are harvested, have adequate sample sizes, and are either mostly mature or mostly immature). Sizes were binned into 5-cm classes. Dotted line indicates length at first maturity. n ¼ total number.
combination of boulder, cobble, and brachiopods correlated best with the transect species patterns. The single habitat that best matched the transect species patterns was boulder (r ¼ 0.63). 4. Discussion An occupied submersible proved to be an effective tool to survey demersal habitats and assemblages of fishes on the continental shelf off central California. This tool provided detailed in situ viewing by observers and additional viewing from the associated video images. The combined use of the observer and the video tape resulted in higher accuracy of fish identification and enumeration. From within the submersible, observers were able to identify small species (Yoklavich and O’Connell, 2008; Love et al., 2009), many of which would not have been identifiable by the video tape alone (i.e., produced from remotely operated vehicles or tow cameras). Despite the high diversity and numbers of small fishes occurring in
our study site, we were able to identify a large percentage of them to species using this tool. Total fish densities in this study were somewhat similar to those estimated using the same submersible in similar habitats and depths elsewhere along the Pacific shelf. Stein et al. (1992) reported an average density of 0.3 fish m2 in boulder habitat and 0.2 fish m2 in mud in surveys off Oregon, while densities in this study were 0.2 fish m2 in both boulder and mud habitats. In southern Monterey Bay, Anderson and Yoklavich (2007) reported higher densities (1.4 fish m2) in high relief rock, but similar density in low relief sediments (0.1 fish m2). Love and Schroeder (2007), surveying high relief, rocky outcrops in southern California, reported densities for all species combined at about 2 fish m2, with squarespot rockfish accounting for a minimum of 78% of all fish. It may be that rocky substrata in northern areas (including the Davenport shelf) are less productive than areas to the south or that rockfish densities are high around high relief as compared to the
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637 Table 4 Habitat selectivity index for 34 species (or species groups) that comprised at least 5% of the total abundance on a single transect. A positive index indicates the species was more abundant than randomly expected and a negative value indicates that species abundance was lower than randomly expected in each of the 4 primary habitats. Bolded text identifies those species having distributions not significantly different from random (P > 0.05). Species
Boulder
Brachiopod
Cobble
Mud
Blackeye goby Bocaccio Calico rockfish Canary rockfish Dover sole English sole Flatfish (unidentified) Greenspotted rockfish Greenstriped rockfish Hagfish (unidentified) Halfbanded rockfish Icelinid sculpin Kelp greenling Lingcod Petrale sole Pink seaperch Poacher (unidentified) Pygmy rockfish Rex sole Rock sole Ronquil Rosy rockfish Sanddab (unidentified) Sculpin (unidentified) Sebastomus (unidentified) Shortspine combfish Squarespot rockfish Starry rockfish Stripetail Threadfin sculpin Vermilion rockfish Widow rockfish Yellowtail rockfish YOY rockfish
23.1 56.7 12.5 50.4 20.5 32.0 28.9 0.9 23.7 18.7 10.1 33.0 25.1 19.0 33.0 2.4 32.5 54.3 33.0 21.9 49.3 50.7 32.5 11.6 29.5 7.6 54.2 57.4 20.5 33.0 42.6 15.0 47.5 39.1
7.5 8.0 8.0 8.0 4.5 6.1 2.8 2.0 14.2 34.9 1.2 8.0 1.0 5.7 8.0 5.5 6.4 7.9 8.0 29.0 3.8 7.8 8.0 4.4 6.2 3.9 8.0 7.2 29.5 8.0 6.8 8.0 7.9 7.8
0.1 6.0 12.2 6.0 6.0 5.0 3.0 2.0 0.4 6.0 31.4 12.2 6.0 2.6 6.0 4.1 6.0 1.0 6.0 1.4 6.0 0.7 5.0 4.7 7.8 11.9 0.1 3.9 6.5 6.0 4.8 6.0 1.1 0.4
15.8 42.7 16.6 36.4 22.0 43.1 34.7 4.9 10.0 10.1 22.5 28.8 18.1 22.1 47.0 12.0 44.8 47.4 47.0 8.6 39.5 43.6 45.5 11.3 31.0 8.2 8.0 46.3 15.5 47.0 31.0 1.0 38.6 31.8
relatively low relief boulder habitat in our study. Fish densities in our study were similar to those in a nearby deepwater canyon (>100 m depth; 0.2 fish m2) (Yoklavich et al., 2000), while fish densities from waters deeper than 100 m off Big Creek Marine Reserve (a remote area off central California that has received relatively little fishing) were somewhat higher ranging from 0.3 to 0.5 fish m2 (Yoklavich et al., 2002). The most common species, pygmy rockfish and blackeye gobies, also are abundant in other locations on the continental shelf. These two species have similar distributions from Canada to Baja California (Eschmeyer et al., 1983; Love et al., 2002). Pygmy rockfish were the most abundant species occurring on rock habitat in southern Monterey Bay, California (Anderson and Yoklavich, 2007), and on Heceta Bank, Oregon (Stein et al., 1992). Pygmy rockfish also were abundant at Big Creek Ecological Reserve in central California (Yoklavich et al., 2002), but not nearly as abundant as in the two other studies. The distribution of pygmy rockfish also extended to deeper depths (>100 m), where it was found to be the third most abundant species off Big Creek (Yoklavich et al., 2002) and twelfth most abundant in a submarine canyon in Monterey Bay (Yoklavich et al., 2000). Blackeye gobies were abundant in surveys from similar depths (Yoklavich et al., 2002; Love et al., 2006; Anderson and Yoklavich, 2007), and were the third most abundant fish species on rocky outcrops in southern California between the depths of 45–50 m (Love and Schroeder, 2007). Blackeye gobies were present, but scarce, in depths >100 m in Monterey Bay (Yoklavich et al., 2000). No mention of blackeye gobies was made from surveys off
635
Table 5 Species that characterize the 15 statistically significant groups of transects (P < 5%). Also indicated are: number of transects (n); the average similarity between all pairs of transects within each group; mean similarity between transects/standard deviation (SD), a measure of the consistency with which a species contributes to the similarity within transects (high value ¼ consistent presence of a species); the percent contribution of a species to the overall similarity of the transects within a group. The most abundant habitat for each group is also indicated to help with interpretation of the species groups. Species
Mean similarity/SD
%Contribution
Group f (n ¼ 2, ave. similarity ¼ 78%, Boulder habitat) Pygmy rockfish * Greenstriped rockfish * Greenspotted rockfish * Lingcod * Bocaccio * Rosy rockfish * Flatfish (unidentified) * Rockfish (unidentified) * Starry rockfish * Sebastomus spp. *
21.6 11.3 10.4 8.7 8.3 7.7 7.2 7.0 6.1 6.1
Group i (n ¼ 13, ave. similarity ¼ 72%, Boulder habitat) Pygmy rockfish 5.7 Yellowtail rockfish 6.4 Rosy rockfish 5.8 Sebastomus spp. 9.5 Blackeye goby 4.4 Rockfish (unidentified) 2.0 Starry rockfish 2.3 Squarespot rockfish 1.3
19.0 11.9 11.6 10.9 10.5 7.8 7.4 6.5
Group c (n ¼ 2, ave. similarity ¼ 71%, Boulder habitat) Blackeye goby * Rosy rockfish * Sebastomus spp. * Yellowtail rockfish * Flatfish (unidentified) * Kelp greenling * Rockfish (unidentified) * Sculpin (unidentified) *
17.2 14.8 12.4 11.3 9.5 9.5 9.5 8.0
Group d (n ¼ 6, ave. similarity ¼ 77%, Boulder habitat) Blackeye goby 10.9 Rosy rockfish 12.4 Northern ronquil 6.3 Yellowtail rockfish 14.2 Flatfish (unidentified) 11.1 Lingcod 10.5 Starry rockfish 5.7 Sanddab (unidentified) 1.3 Sebastomus spp. 1.4 Rockfish (unidentified) 1.4
16.4 14.3 10.2 9.7 8.1 7.7 6.6 5.9 4.8 4.7
Group g (n ¼ 2, ave. similarity ¼ 76%, Boulder habitat) Blackeye goby * Rockfish (unidentified) * Rosy rockfish * Sebastomus spp. * Greenspotted rockfish * Starry rockfish *
20.0 17.9 17.8 14.1 11.2 9.6
Group j (n ¼ 4, ave. similarity ¼ 76%, Boulder habitat) Rosy rockfish 30.6 Blackeye goby 5.7 Yellowtail rockfish 8.6 Starry rockfish 9.4 Rockfish (unidentified) 12.5 Sebastomus spp. 12.5 Greenspotted rockfish 15.0 Vermilion rockfish 6.8 Bocaccio 3.6
12.7 12.7 12.5 9.8 9.2 8.9 7.3 7.3 7.0
Group e (n ¼ 2, ave. similarity ¼ 69%, Mud/Boulder habitat) Rosy rockfish *
15.0
(continued on next page)
636
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Table 5 (continued )
Table 5 (continued )
Species
Mean similarity/SD
%Contribution
Species
Sanddab (unidentified) Blackeye goby Pink surfperch Starry rockfish Flatfish (unidentified) Yellowtail rockfish Canary rockfish Rockfish (unidentified)
* * * * * * * *
13.4 13.1 9.8 9.5 9.1 8.5 7.2 7.2
Group m (n ¼ 4, ave. similarity ¼ 64%, Mud/Cobble habitat) Greenstriped rockfish 4.4 Greenspotted rockfish 4.4 Flatfish (unidentified) 2.9 Sanddab (unidentified) 3.9 Sebastomus spp. 7.4 Sculpin (Icelinus spp.) 9.4 Sculpin (unidentified) 6.5
Group k (n ¼ 24, ave. similarity ¼ 70%, Mud/Boulder habitat) Blackeye goby 4.8 Rosy rockfish 5.0 Yellowtail rockfish 5.8 Greenspotted rockfish 5.3 Sebastomus spp. 2.7 Rockfish (unidentified) 2.1 Starry rockfish 2.2 Lingcod 2.1 Greenstriped rockfish 1.7
13.7 10.7 10.5 10.5 8.6 7.4 6.4 6.3 6.3
Group o (n ¼ 10, ave. similarity ¼ 68%, Mud/Boulder habitat) Blackeye goby 9.0 Greenspotted rockfish 10.4 Greenstriped rockfish 4.6 Flatfish (unidentified) 7.6 Rosy rockfish 1.9 Pink surfperch 1.3 English sole 1.3
16.6 14.3 11.5 10.7 9.3 6.2 5.5
Group b (n ¼ 2, ave. similarity ¼ 87%, Mud habitat) Flatfish (unidentified) * Poacher (unidentified) * Sanddab (unidentified) * Greenstriped rockfish * Rex sole * English sole *
20.4 20.3 17.8 15.5 13.0 13.0
Group n (n ¼ 3, ave. similarity ¼ 69%, Mud habitat) Greenstriped rockfish 29.4 Greenspotted rockfish 5.6 Flatfish (unidentified) 10.2 English sole 4.4 Lingcod 12.4 Poacher (unidentified) 5.9 Sebastomus spp. 15.1 Rock sole 73.8
18.5 12.4 12.3 9.5 9.3 9.1 8.8 8.5
Group p (n ¼ 19, ave. similarity ¼ 69%, Mud habitat) Flatfish (unidentified) 6.3 Sanddab (unidentified) 7.3 Poacher (unidentified) 5.5 Greenstriped rockfish 2.6 English sole 1.8 Blackeye goby 1.9 Greenspotted rockfish 1.8 Pink surfperch 1.5
15.4 14.6 14.1 10.8 10.2 10.1 9.5 8.6
Group l (n ¼ 6, ave. similarity ¼ 60%, Greenstriped rockfish Flatfish (unidentified) Greenspotted rockfish Lingcod Pink surfperch
24.5 19.7 19.1 11.0 9.2
Oregon (Pearcy et al., 1989; Stein et al., 1992), which were in slightly deeper water and may be below the depth range of this species in the north. These data indicate that pygmy rockfish and blackeye gobies are abundant throughout much of their range. Utilization of brachiopod beds as a fish habitat has not been reported prior to this study. Brachiopods occur in a turbid area of the continental shelf on a thin mud bottom, attaching themselves to both living and dead conspecifics (Pennington et al., 1999). This habitat type had the lowest abundance and diversity of fishes, and only two species (greenspotted and greenstriped rockfishes) were commonly observed in and around brachiopods; a few other species, such as small flatfishes and lingcod also were occasionally seen. It may be that brachiopod beds are not associated with suitable prey or perhaps the beds are an ephemeral habitat that is periodically covered by the surrounding sediment and not consistently available as shelter for these fishes. Fishes less than 20 cm accounted for over 80% of all fish observed during our survey. Most of the large species (>25 cm as adults) were represented by small, immature individuals. This occurred across species groups, including rockfishes, flatfishes, and lingcod. The absence of large fishes was not unique to this area. Love et al. (2006) found most individuals of vermilion, flag (S. rubrivinctus), and greenspotted rockfishes were immature during a survey off southern California in waters from 75–79 m deep. In a study on the southern side of Monterey Bay, Anderson and Yoklavich (2007) observed more small (<20 cm) commercially important species than larger individuals. Yoklavich et al. (2000) reported that most greenspotted rockfish were immature from areas <175 m; however, at deeper depths most of the rockfishes were mature. Yoklavich et al. (2002) reported that young-of-theyear rockfishes accounted for 30–82% of the total fish surveyed in water depths <100 m, but represented only 0.7–1.9% of the total fish counted in water depths >100 m. The abundance of immature fishes may indicate that this area of the shelf is a nursery for younger fishes. In a study off Oregon, Pearcy et al. (1989) suggested that a nursery ground for young rockfishes was located on the top of the offshore Heceta Bank (100 m). Love and Schroeder (2007) reported relatively few large individuals of large species on rocky outcrops from 45–50 m water depth, and suggested that larger individuals migrated to deeper water. Many fish species exhibit ontogenetic habitat shifts (Hallacher and Roberts, 1985; Johnson et al., 2001; Love et al., 2006; Love and Yoklavich, 2008). Auster et al. (2003) observed juvenile Acadian redfish (Sebastes fasciatus) on Stellwagen Bank in different habitats than the adults, leading the authors to surmise that the surveyed area could be a recruitment habitat. Four flatfish species were found to have ontogenetic shifts in habitat (mainly in depth) in the Gulf of Maine (Methratta and Link, 2007). Juvenile pollock (Theragra chalcogramma) have been shown to live in shallow nursery areas off Japan and in the Bering Sea before moving to deeper adult habitats (Nishimura et al., 2007; Winter et al., 2007). The young of many species (rockfishes, lingcod, and flatfishes) recruit from the plankton to shallow areas and move deeper to adult habitat as they grow (Love et al., 2002). Our study site on the
Mud/Brachiopod habitat) 7.6 5.4 9.2 1.3 1.4
Group q (n ¼ 11, ave. similarity ¼ 64%, Mud/Brachiopod habitat) Greenspotted rockfish 5.4 Greenstriped rockfish 4.7 Lingcod 5.0 Blackeye goby 1.9 Sebastomus spp. 2.0 Shortspine combfish 2.0 Flatfish (unidentified) 1.3
17.1 16.4 12.0 11.7 8.8 8.2 7.4
Mean similarity/SD
%Contribution 16.0 14.4 11.6 11.6 11.5 10.1 10.0
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
shelf may be an intermediate staging area between the shallow, nearshore young-of-the-year habitats and deeper, adult habitats. It also is possible that the lack of mature fishes is due to past fishing pressure and that populations in this area have not yet recovered. The study area has been closed to recreational fishing and has received limited commercial fishing since 2002 (PFMC, 2003). Prior to that time, this area had been fished heavily by both commercial trawl and longline gear as well as recreational fishermen for at least 100 years. Baskett et al. (2006) suggested that, in areas where large predatory fishes were removed and small species dominate, stock recovery of the larger species may be slowed due to competition for food and shelter resources between the juveniles of the once dominant larger species and the small-sized species. Unfortunately, no prior visual survey data are available from this area, and comparison with commercial and recreational catches would under-represent the small fishes that were so prevalent in our study. This study provides post-fishery baseline data and additional visual surveys will be needed to monitor the potential recovery of this shelf assemblage as time of protection increases. These additional surveys will be invaluable in determining whether these habitats can support populations of mature fishes. Relatively few habitat surveys have focused on the intermediate depths (30–100 m) of the continental shelf off the west coast of the United States. This area may be an important nursery ground and may replenish deeper areas with maturing fishes. Knowledge of the fish and habitat associations at different life stages is critical in determining the placement of marine protected areas and in rebuilding stocks. Any ecosystem-based management objectives should consider vital areas such as this study site. Using fish–habitat associations, combined with broad-scale seafloor habitat maps, could improve our groundfish stock assessments for several species. Acknowledgments We thank the crews of the R/V Velero IV and the Delta submersible for their fine work during this study. We also thank Linda Snook and John Field for help with submersible observations, and Lisa Wooninck and Zoe Schumacher for logistical help during the cruise. We thank E.J. Dick for help in statistical matters, and S. Sogard, J. Mason, and K. Sakuma for their comments on earlier drafts of the manuscript. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.ecss.2009.05.008. References Anderson, T.J., Yoklavich, M.M., 2007. Multi-scale habitat associations of deep-water demersal fishes off central California. Fishery Bulletin 105, 168–179. Auster, P.J., Lindholm, J., Valentine, P.C., 2003. Variation in habitat use by juvenile Acadian redfish, Sebastes fasciatus. Environmental Biology of Fishes 68, 381–389. Baskett, M.L., Yoklavich, M., Love, M.S., 2006. Predation, competition, and the recovery of exploited fish stocks in marine reserves. Canadian Journal of Fish and Aquatic Science 63, 1214–1229. Bray, J.R., Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27, 325–349. Carr, M.H., 1991. Habitat selection and recruitment of an assemblage of temperate zone reef fishes. Journal of Experimental Marine Biology and Ecology 146, 113–137. Christensen, V., Guenette, S., Heymans, J.J., Walters, C.J., Watson, R., Zeller, D., Pauly, D., 2003. Hundred-year decline of North Atlantic predatory fishes. Fish and Fisheries 4, 1–24. Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK, 91 pp. Cormack, R.M., 1971. A review of classification. Journal of the Royal Statistical Society Series A 134, 321–367.
637
DeMartini, E.E., Roberts, D.A., 1990. Effects of giant kelp (Macrocystis) on the density and abundance of fish in a cobble-bottom kelp forest. Bulletin of Marine Science 46, 287–300. Echeverria, T.W., 1987. Thirty-four species of California rockfishes: maturity and seasonality of reproduction. Fishery Bulletin 85, 229–250. Eschmeyer, W.N., Herald, E.S., Hammann, H., 1983. Pacific Coast fishes. Houghton Mifflin, Co, Boston, MA, 336 pp. Eittreim, S.L., Anima, R.J., Stevenson, A.J., 2002. Seafloor geology of the Monterey Bay area continental shelf. Marine Geology 181, 3–34. Fishbase, 2007. Shortspine combfish Web Page. http://www.fishbase.org. Greene, H.G., Yoklavich, M.M., Starr, R.M., O’Connell, V.M., Wakefield, W.W., Sullivan, D.E., McRea, J.E., Cailliet, G.M., 1999. A classification scheme for deep seafloor habitats. Oceanologica Acta 22, 663–678. Hallacher, L.E., Roberts, D.A., 1985. Differential utilization of space and food by inshore rockfishes (Scorpaenidae: Sebastes) of Carmel Bay, California. Environmental Biology of Fishes 12, 91–110. Hart, J.L., 1973. Pacific Fishes of Canada. Fisheries Research Board of Canada, Ottawa, 740 pp. Johnson, K.A., Yoklavich, M.M., Cailliet, G.M., 2001. Recruitment of three species of juvenile rockfish (Sebastes spp.) on soft benthic habitat in Monterey Bay, California. CalCOFI Reports 42, 153–166. Laidig, T.E., Chess, J.R., Howard, D.F., 2007. Relationship between abundance of juvenile rockfishes (Sebastes spp.) and environmental variables documented off northern California and potential mechanisms for the covariation. Fishery Bulletin 105, 39–48. Love, M.S., 1996. Probably More than you Want to Know about the Fishes of the Pacific Coast. Really Big Press, Santa Barbara, CA, 381 pp. Love, M.S., Schroeder, D.M., 2007. A characterization of the fish assemblage of deep photic zone rock outcrops in the Anacapa Passage, southern California, 1995 to 2004, with evidence of a regime shift. CalCOFI Reports 48, 165–176. Love, M.S., Yoklavich, M.M., 2008. Habitat characteristics of juvenile cowcod, Sebastes levis (Scorpaenidae), in southern California. Environmental Biology of Fishes 82, 195–202. Love, M.S., Yoklavich, M., Thorsteinson, L., 2002. The Rockfishes of the Northeast Pacific. University of California Press, Berkeley and Los Angeles, CA, 405 pp. Love, M.S., Schroeder, D.M., Lenarz, B., Cochrane, G.R., 2006. Gimme shelter: the importance of crevices to some fish species inhabiting a deeper-water rocky outcrop in southern California. CalCOFI Reports 47, 119–126. Love, M.S., Yoklavich, M., Schroeder, D.M., 2009. Demersal fish assemblages in the southern California Bight based on visual surveys in deep water. Environmental Biology of Fishes 84, 55–68. Methratta, E.T., Link, J.S., 2007. Ontogenetic variation in habitat associations for four flatfish species in the Gulf of Maine-Georges Bank region. Journal of Fish Biology 70, 1669–1688. Nishimura, A., Hamatsu, T., Shida, O., Mihara, I., Mutoh, T., 2007. Interannual variability in hatching period and early growth of juvenile walleye Pollock, Theragra chalcogramma, in the Pacific coastal area of Hokkaido. Fisheries Oceanography 16, 229–239. Paddock, M.J., Estes, J.A., 2000. Kelp forest fish populations in marine reserves and adjacent exploited areas of central California. Ecological Applications 10, 855–870. Parker, S.J., Berkeley, S.A., Golden, J.T., Gunderson, D.R., Heifetz, J., Hixon, M.A., Larson, R., Leaman, B.M., Love, M.S., Musick, J.A., O’Connell, V.M., Ralston, S., Weeks, H.J., Yoklavich, M.M., 2000. Management of Pacific Rockfish. Fisheries 25, 22–29. Pearcy, W.G., Stein, D.L., Hixon, M.A., Pikitch, E.K., Barss, W.H., Starr, R.M., 1989. Submersible observations of deep-reef fishes of Heceta Bank, Oregon. Fishery Bulletin 87, 955–965. Pennington, J.T., Tamburri, M.N., Barry, J.P., 1999. Development, temperature tolerance, and settlement preference of embryos and larvae of the articulate brachiopod Laqueus californianus. Biological Bulletin 196, 245–256. PFMC (Pacific Fishery Management Council), 2003. Final environmental impact statement for the proposed groundfish acceptable biological catch and optimum yield specifications and management measures: 2003 Pacific Coast Groundfish Fishery, Portland OR, 206 pp. Phillips, J.B., 1964. Life history studies on ten species of rockfish (Genus Sebastodes). California Department of Fish and Game Fish Bulletin 126, 70 pp. Rothrock, G.C., 1973. Age-length, weight, fecundity, and meristics of the kelp greenling (Hexagrammos decagrammus) off California. M.S. Thesis, University of California, Davis, 95 pp. Stein, D.L., Tissot, B.N., Hixon, M.A., Barss, W., 1992. Fish–habitat associations on a deep reef at the edge of the Oregon continental shelf. Fishery Bulletin 90, 540–551. Winter, A., Coyle, K.O., Swartzman, G., 2007. Variations in age-0 pollock distribution among Bering Sea nursery areas: A comparative study through acoustic indices. Deep Sea Research (Part II, Topical Studies in Oceanography) 54, 2869–2884. Yoklavich, M.M., O’Connell, V., 2008. Twenty years of research on demersal communities using the Delta submersible in the northeast Pacific. In: Reynolds, J.R., Greene, H.G. (Eds.), Alaska Sea Grant College Program. University of Alaska Marine habitat mapping technology for Alaska, Fairbanks, pp. 143–155. Yoklavich, M.M., Greene, H.G., Cailliet, G.M., Sullivan, D.E., Lea, R.N., Love, M.S., 2000. Habitat association of deep-water rockfishes in a submarine canyon: an example of a natural refuge. Fishery Bulletin 98, 625–641. Yoklavich, M.M., Cailliet, G.M., Lea, R.N., Greene, H.G., Starr, R.M., de Marignac, J., Field, J., 2002. Deepwater habitat and fish resources associated with the Big Creek Marine Ecological Reserve. CalCOFI Reports 43, 120–140.
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Demersal fish and habitat associations from visual surveys on the central California shelf Thomas E. Laidig*, Diana L. Watters, Mary M. Yoklavich Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, 110 Shaffer Road, Santa Cruz, CA 95060, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 August 2008 Accepted 12 May 2009 Available online 20 May 2009
In 2004, we surveyed demersal fishes and habitats on the continental shelf off central California (65–110 m depth) using the occupied submersible Delta. Our objectives were to estimate the relative abundance of habitats and to examine demersal fish species composition, diversity, density, and sizes relative to these habitats. A total of 112 transects were completed covering 32 km of seafloor. A higher density of fishes was estimated in boulder and cobble habitats than in mud and brachiopod beds. More than 80% of the fishes were small, measuring 20 cm or less in total length. Species with small maximum size (primarily pygmy rockfish, Sebastes wilsoni, and blackeye gobies, Rhinogobiops nicholsii) accounted for nearly half (49%) of the total number of 12,441 fishes. Most fishes were immature, with only 4 of 20 harvested species having more than 50% of the individuals larger than the size at first maturity. Our study area on the continental shelf may be an ontogenetic transition zone for immature fishes before they move to their adult habitat on the slope. Alternatively, historical fishing pressure may have contributed to the lack of large, mature fishes in the survey area. Understanding the importance of these habitats to fishes at various life stages will improve our ability to assess these deepwater fish stocks and effectively manage these living resources on an ecosystem basis. Published by Elsevier Ltd.
Keywords: demersal fishes continental shelf Delta submersible habitat habitat selection community structure
1. Introduction Fish habitat requirements are fundamental to sound fisheries management, particularly in establishing and monitoring effective protected areas. However, many demersal shelf species live at depths that are difficult to study (e.g., >30 m), thereby limiting our understanding of these fishes and their associated habitats. Populations of several demersal species have been declining for years in the northeast Pacific and North Atlantic (Parker et al., 2000; Christensen et al., 2003). Understanding the habitat associations for these species is an important component to developing successful rebuilding plans. Researchers have used quantitative survey methods to gather some information on demersal fishes and their habitats along the West Coast of North America. Much of this work has been conducted from an occupied submersible on offshore banks and in submarine canyons deeper than 100 m (Pearcy et al., 1989; Stein et al., 1992; Yoklavich et al., 2000; Love et al., 2009). Other fish habitat studies have been conducted using SCUBA in waters shallower than 30 m (DeMartini and Roberts, 1990; Carr, 1991; Paddock
* Corresponding author. E-mail address: [email protected] (T.E. Laidig). 0272-7714/$ – see front matter Published by Elsevier Ltd. doi:10.1016/j.ecss.2009.05.008
and Estes, 2000; Laidig et al., 2007). Only a few surveys of fish– habitat associations have been conducted at intermediate depths (30–100 m) on the continental shelf (Yoklavich et al., 2002; Anderson and Yoklavich, 2007; Love and Schroeder, 2007). In this paper, we report on surveys of demersal fishes and habitats at these intermediate depths on the continental shelf off central California using the occupied submersible Delta. This area has been fished since the late 1800s and was closed to most bottom fishing in 2002 (PFMC, 2003), providing an opportunity to develop an early post-fishing baseline. Our objectives were to estimate the relative abundance of habitats and to examine demersal fish species and size composition, diversity, and density relative to these habitats. 2. Methods 2.1. Study site Surveys were conducted on the continental shelf north of Monterey Bay approximately 11 km southwest of Davenport, California (Fig. 1). The study area was 18 km long and 3 km wide (36 520 to 37 020 N; 122110 to 122190 W), and ranged in depth from 65 to 110 m. Much of the sea floor in the study area consisted of soft mud. We focused our surveys in areas of likely habitats of
630
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Fig. 1. Map of the study area off central California. The submersible transects are displayed as colored lines, with each color representing one of the four primary habitats (boulder, cobble, mud, and brachiopod). The dark green Purisima mudstone formation represents the interpreted hard substratum (from Eittreim et al., 2002). Inset: An example of the distribution of different habitat types along a segment of a submersible transect.
Pacific rockfishes (Sebastes spp.) (i.e., hard substratum is dark green in Fig. 1), and locations of previous research longline surveys conducted from 2001to 2004 (D. Pearson, NMFS, Santa Cruz, CA, pers. comm.). 2.2. Fish and habitat surveys Surveys were conducted from 23 August to 4 September 2004 between 07:00 and 17:30 h using the Delta, a 4.6 m-long
submersible that accommodates one scientific observer and one pilot. Survey dates were selected based on the availability of the submersible and consistently calm sea state to maximize survey effort. Three experienced observers collected all data. Up to six 10-min transects were completed during each dive. The direction and location of each transect were guided by scientists monitoring the submersible’s position and communicating with the pilot from the surface support vessel R/V Velero IV. Between each transect, the submersible would run for at least 5 min to a new sampling area
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
determined by the scientist on the Velero IV. The Delta’s position was continuously recorded using WinFrog navigation software and the ORE Trackpoint Ultra Short Base Line system. Navigation data were subsequently edited for outliers and interpolated to onesecond intervals. Transects were later plotted and measured using ArcMap 9.0 GIS software. The submersible traveled at an average speed of 0.9 knots (dependent on the bottom topography), approximately 1 m above the bottom. Three video cameras documented benthic fauna during each dive. One external color camera was mounted above the middle view port on the starboard side of the submersible and recorded habitats and organisms up to approximately 1.5 m above the seafloor. A low-light, black-and-white external camera was aimed forward to view upcoming fishes and terrain. The third camera was located inside the submersible and pointed downward so as to document fauna from the lowest view port on the starboard side. This camera was used to record fishes closest to the submersible along the transect’s inside edge. The scientific observer conducted belt–transect surveys through the middle view port, orally recording onto the three videotapes all fishes observed within two meters of the submersible. The 2-m width of the transect was verified using a hand-held sonar gun. Fishes were identified to the lowest possible taxon and counted. Total length of fishes was estimated using the aide of two parallel lasers mounted 20 cm apart on either side of the middle view port camera as a reference scale. The video footage for each transect was later reviewed and observations confirmed. From this review and the audio-recordings, data were transcribed into a database. Bottom habitat was characterized from the videotapes, using the geological habitat classification system of Greene et al. (1999). Habitat comprised four main substrata: boulder (>25 cm wide), cobble (<25 cm wide), mud, and brachiopod beds, Laqueus californianus. If a substratum covered >50% of the seafloor it was considered the primary habitat. Changes in habitat classification were noted only if they persisted for longer than 3 s on the video transect (the time for an image to move completely across the video monitor, about 1.4 m substrate length). Anderson and Yoklavich (2007) determined that very little information (related to fish–habitat associations) was lost by eliminating these small-scale patches of habitat. Brachiopods occurred individually, in small groups, and in large aggregations (numbering thousands of individuals) attached to hard substrata (e.g., cobbles, boulders, and other brachiopods), which were often covered by a thin layer of mud. We only considered the large, bed-forming aggregations (Fig. 2) covering >50% of the seafloor as a primary habitat in this study.
2.3. Data analysis Those species comprising 5% or more of fishes counted on any given transect were used in statistical analyses. Using this criterion, species that were rare overall but important in the assemblage of specific transects were included in the analysis. Additionally, we noted those species that commonly are recreationally and commercially harvested at this location. A Durbin–Watson statistic was used to test for independence of fish densities between the transects. We examined species associations with habitats by calculating a habitat selectivity index. Because habitat types were not equally abundant, we standardized habitat use to habitat availability by subtracting proportional occurrence of each habitat type from the proportional abundance of each species on that habitat (Anderson and Yoklavich, 2007). We used a chi-square goodness of fit test to determine if species were randomly distributed among habitats.
631
Fig. 2. A large aggregation of brachiopods (Laqueus californianus) off Davenport, CA, in 100 m depth. A small (15 cm total length) greenspotted rockfish (Sebastes chlorostictus) is in the background.
Size distribution was examined for each species by pooling lengths in 5-cm bins. Length at first maturity was established using published data (Phillips, 1964; Hart, 1973; Rothrock, 1973; Echeverria, 1987; Love, 1996; Love et al., 2002; Fishbase, 2007). We chose length at first maturity as a more conservative indicator than length at 50% maturity. No species groups were used due to differences in length at first maturity within these groups. A matrix of species densities (number m2) by transect was constructed for multivariate analysis of species assemblages. Densities were fourth-root transformed to down-weight highly abundant species and to allow the full spectrum of species to contribute to the analysis. Multivariate analyses were performed using PRIMER 6 software (Clarke and Gorley, 2006) to describe associations among fish species and habitat types. Similarities in species densities were calculated for every pair of transects using the Bray-Curtis coefficient (Bray and Curtis, 1957). The resulting similarity matrix was used in a hierarchal cluster analysis (Cormack, 1971) (group–average linking). Similarity profile (SIMPROF) permutation tests were incorporated into the cluster analysis (Clarke and Gorley, 2006) to test each node of the dendrogram for statistically significant groups. Significant groups (p < 5%) were analyzed with a similarity percentage routine (SIMPER) to identify the species that characterized those groups. The SIMPER routine calculated the average similarity between all pairs of transects within each group and determined the contribution that species made to that similarity in two ways: (1) measuring the consistency with which a species contributed (average similarity between transects/standard deviation; high value ¼ consistent presence of a species); and (2) the
Table 1 Mean area and fish density (with standard error in parentheses) for each primary habitat type. Habitat type
Mud Boulder Brachiopod Cobble
Mean area
Mean fish density
(m2)
(#/m2)
151 94 23 18
0.15 (0.03) 0.24 (0.05) 0.02 (0.005) 0.10 (0.03)
(10) (8) (5) (3)
632
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Table 2 Total number, total relative abundance (%), highest percent on any single transect (% highest), and mean total length and standard error (SE) of fish taxa observed from the Delta submersible, summer 2004. Names in bold signify that they were at least 5% of the total fish abundance on any given transect. Common name
Pygmy rockfish Blackeye goby Rosy rockfish Greenspotted rockfish Yellowtail rockfish Greenstriped rockfish Sebastomus YOY rockfish Sanddab spp. Unidentified flatfish Squarespot rockfish Starry rockfish Lingcod Unidentified poacher Pink seaperch Canary rockfish Halfbanded rockfish English sole Bocaccio Northern ronquil Vermilion rockfish Unidentified rockfish Shortspine combfish Copper rockfish Kelp greenling Flag rockfish Unidentified sculpin Rock sole Widow rockfish Speckled rockfish Brown rockfish Slender sole Petrale sole Rosethorn rockfish Calico rockfish Unidentified sculpin Spotfin sculpin Blue rockfish Dover sole Stripetail rockfish Unidentified hagfish Unidentified skate Painted greenling Rex sole Yelloweye rockfish Longspine combfish Threadfin sculpin Cowcod Longnose skate Spotted cusk-eel Unidentified combfish Big skate Greenblotched rockfish Plainfin midshipman Ratfish Starry skate Unidentified prickleback California halibut Northern anchovy Redbanded rockfish Unidentified salmon Wolfeel
Scientific name
Sebastes wilsoni Rhinogobiops nicholsii Sebastes rosaceus Sebastes chlorostictus Sebastes flavidus Sebastes elongatus Sebastomus Sebastes spp. (YOY) Citharichthys spp. Pleuronectidae Sebastes hopkinsi Sebastes constellatus Ophiodon elongatus Agonidae Zalembius rosaceus Sebastes pinniger Sebastes semicinctus Pleuronectes vetulus Sebastes paucispinis Ronquilus jordani Sebastes miniatus Sebastes spp. Zaniolepis frenata Sebastes caurinus Hexagrammos decagrammus Sebastes rubrivinctus Cottidae Lepidopsetta bilineata Sebastes entomelas Sebastes ovalis Sebastes auriculatus Lyopsetta exilis Eopsetta jordani Sebastes helvomaculatus Sebastes dallii Icelinus spp. Icelinus tenuis Sebastres mystinus Microstomus pacificus Sebastes saxicola Myxinidae Rajidae Oxylebius pictus Errex zachirus Sebastes ruberrimus Zaniolepis latipinnis Icelinus filamentosus Sebastes levis Raja rhina Chilara taylori Zaniolepis spp. Raja binoculata Sebastes rosenblatti Porichthys notatus Hydrolagus colliei Raja stellulata Stichaeidae Paralichthys californicus Engraulis mordax Sebastes babcocki Oncorhynchus spp. Anarrhichthys ocellatus
Total number
2897 2191 1130 809 730 627 509 466 393 366 344 240 204 182 157 145 131 103 97 96 82 77 67 44 43 37 28 27 25 19 18 15 12 12 11 11 9 8 8 8 7 7 6 6 6 5 4 3 3 3 3 2 2 2 2 2 2 1 1 1 1 1 12448
percent contribution of a species to the overall similarity of the group. We used non-metric multidimensional scaling (MDS) to further examine species assemblages among transects. A stress value indicates the degree of difficulty in constraining the relationships
% Total
23.4 17.7 9.1 6.5 5.9 5.1 4.1 3.8 3.2 3.0 2.8 1.9 1.6 1.3 1.3 1.2 1.0 0.7 0.7 0.7 0.6 0.6 0.5 0.4 0.3 0.3 0.2 0.2 0.2 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 100.0
% Highest
79.5 55.0 31.1 41.8 25.8 5.7 28.1 44.4 84.8 40.0 7.9 27.4 12.9 47.7 15.4 22.0 54.0 29.0 6.7 10.9 9.1 1.8 10.6 3.9 5.8 3.6 6.8 5.7 16.4 3.3 4.4 3.8 5.1 3.4 8.6 7.0 2.9 3.9 5.6 5.9 11.1 3.7 1.1 5.0 1.0 2.8 7.0 1.8 2.9 2.0 2.9 1.9 1.4 3.8 1.1 1.4 1.4 3.8 4.7 1.7 1.4 0.5
Mean length
Length
(cm)
(SE)
9.1 7.3 16.5 19.2 27.9 12.9 10.2 5 11.0 12.7 15.1 20.0 36.2 11.4 12.8 32.2 14.5 20.0 42.5 10.4 33.9 13.8 16.8 34.3 28.3 21.4 8.4 17.5 26.8 25.6 25.9 13.7 16.3 19.5 13.6 9.5 10.6 25 16.9 10.6 17.5 37 11.7 16.7 32.5 17 7.5 46.7 40 10 13.3 35 32.5 12.5 50 42.5 10 40 10 20 50 20
0.0 0.1 0.1 0.3 0.2 0.2 0.3 0.01 0.3 0.3 0.2 0.4 0.8 0.3 0.2 0.8 0.3 0.5 1 0.3 0.7 0.8 0.5 0.7 0.5 1 0.7 1 1.1 0.9 1.4 0.9 2.3 1.3 0.9 1.3 1 0 1.3 1.8 2.5 6.6 1.1 1.7 3.1 2.5 2.5 6 0 0 3.3 5 2.5 2.5 N/A 2.5 N/A N/A N/A N/A N/A N/A
into low dimensional space (i.e., stress values <0.1 indicate relatively good ordination, whereas values >0.3 indicate relatively poor ordination). PRIMER global BEST match-permutation test was used to evaluate a null hypothesis of no agreement in multivariate patterns among species and habitats from the same transects. This
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
633
Table 3 Length at first maturity (total length, cm) for 22 species comprising at least 5% of the total abundance on any given transect. Number and percent of fishes less than or equal to length at first maturity are indicated. Names in bold signify fish that are harvested. Common name
Length at 1st maturity
Total fish measured
Number less than first maturity
% less than first maturity
Reference
Calico rockfish Bocaccio Shortspine combfish Squarespot rockfish Halfbanded rockfish Canary rockfish Kelp greenling Vermilion rockfish Blackeye goby Widow rockfish Rosy rockfish Greenstriped rockfish Lingcod Greenspotted rockfish Stripetail rockfish Yellowtail rockfish Starry rockfish English sole Rock sole Dover sole Petrale sole Rex sole
7 32 15 13 10 27 29 31 5 26 16 15 40 25 15 30 25 25 28 30 38 17
9 96 67 341 131 105 38 81 2189 25 1120 626 196 798 8 723 235 103 26 8 12 6
0 6 58 66 28 34 16 35 1176 14 652 458 147 686 7 640 209 99 25 8 12 6
0 6 9 19 21 32 42 43 54 56 58 73 75 86 88 89 89 96 96 100 100 100
6 4, 6 7 4, 6 6 2, 1, 4 3 4, 6 5 4, 6 4, 6 4, 6 5 4, 6 4, 6 4, 6 4, 6 2 2 2, 5 2, 5 5
References: 1, Phillips, 1964; 2, Hart, 1973; 3, Rothrock, 1973; 4, Echeverria, 1987; 5, Love, 1996; 6, Love et al., 2002; 7, Fishbase, 2007.
test finds the best match among the species assemblage patterns and habitat types associated with transects. 3. Results A total of 112 transects were completed during 28 dives covering 32 km of seafloor in 12 days (Fig. 1). The Durbin–Watson statistic was 1.9, demonstrating no statistical dependence among the transects. The dominant habitats were mud and boulder, with a mean of 151 and 94 m2 transect1 and representing 53% and 32% of available habitats respectively (Table 1). Brachiopod beds and cobble were much less abundant, representing on average 41 m2 transect1 (14%) of the surveyed seafloor. Mean fish density was highest in boulder habitat (0.24 fish m2), and lowest in brachiopod habitat (0.02 fish m2) (Table 1; Appendix A). A total of 12,448 fishes were observed during this study, with 10,396 (84%) identified to species. Fishes were identified to 62 taxa, including 49 species, 7 genera and subgenera, and 6 families (Table 2). Thirty-four of these taxa comprised at least 5% of the total number of fishes observed on a given transect and therefore were included in further analyses. Small fishes dominated the survey, with 85% measuring 20 cm or less in total length (Table 2). Pygmy rockfish, Sebastes wilsoni (n ¼ 2897), and blackeye goby, Rhinogobiops nicholsii (n ¼ 2191), both non-harvested and small-bodied species, were the two most abundant species. These two small species accounted for 41% of all fishes in this study. Rockfishes accounted for 67% of all fishes and 74% of all fishes 20 cm or less in total length. Of the 22 species for which maturity data have been published, greater than 50% of individuals of 14 species were smaller than or equal to the length at first maturity (Table 3; Fig. 3). Twenty species were classified as harvested, and only 4 of these comprised mostly mature individuals (greater than 50%): kelp greenling (Hexagrammos decagrammus), bocaccio (Sebastes paucispinis), and canary (Sebastes pinniger) and vermilion (Sebastes miniatus) rockfishes. Twenty-eight of the 34 species groups had a non-random habitat-use pattern (chi-square statistic p < 0.05; Table 4). The 6 species that were randomly distributed (indicated with an asterisk on Table 4) all had low sample sizes (n ¼ 4–28 individuals). Most
species were positively associated with boulder habitat, while some species were positively associated with mud (e.g., flatfishes (Pleuronectidae), greenstriped rockfish (Sebastes elongatus), pink surfperch (Zalembius rosaceus), and poachers (Agonidae)). The lowest numbers of species were positively associated with brachiopod beds and cobble. Greenspotted rockfish (Sebastes chlorostictus) were positively associated with all but mud habitats and did not have greater selectivity for any one habitat. Within the cluster analysis, SIMPROF tests identified 17 groups of transects (a–q) that were significant (p < 5%). The MDS ordination, (stress value ¼ 0.15), produced comparable groups to that of the SIMPROF analysis. Two groups (a and h) consisted of single transects and could not be analyzed by SIMPER. One of these was dominated by high numbers of unidentified sanddabs (Citharichthys spp.) (82%), and the other by greenspotted, rosy (Sebastes rosaceus), and squarespot (Sebastes hopkinsi) rockfishes, and blackeye gobies. Within the 15 groups that were analyzed with SIMPER, average percent similarity of transects ranged from 60% to 87% (Table 5). These groups were typified by five to ten species that cumulatively contributed 90% of total similarity, and were consistently abundant throughout the transects in their group, as indicated by mean similarity/SD values. There was a high degree of overlap in species among some groups, with many species occurring in multiple groups. Fish assemblages that occurred over boulder habitat were of two general types (Table 5): one in which pygmy rockfish dominated (19–22% contribution), and the other without pygmy rockfish. Rosy, yellowtail (Sebastes flavidus), and starry rockfishes (Sebastes constellatus), the subgenus Sebastomus, and blackeye gobies were consistent members of both types of assemblage on boulder habitat. Flatfishes, poachers, sanddabs, and greenstriped rockfishes characterized the species assemblages that occurred on muddominated habitat. Assemblages of greenstriped and greenspotted rockfishes, lingcod (Ophiodon elongatus), and blackeye gobies were associated with brachiopod beds. Cobble was dominant in only one instance, preventing an analysis of the assemblages occurring on this habitat. The null hypothesis of no agreement in multivariate pattern between the species and habitat similarity matrices was rejected by the global BEST match test (r ¼ 0.67, p ¼ 0.1%). The
634
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
0.25
Greenspotted rockfish n=798
0.30
Vermilion rockfish n=81
0.25
0.20
0.20 0.15 0.15 0.10 0.10 0.05
0.00
0.05
5
10
15
20
25
30
0.35
35
40
Starry rockfish n=235
0.30
0.00
0.35 0.30
0.25
0.25
0.20
0.20
0.15
0.15
0.10
0.10
0.05
0.05
0.00
5
10
15
20
25
30
0.30 Lingcod n=196
0.25
0.00 0.50 0.45
15
20
25
30
35
40
45
Bocaccio n=96
20
25
30
35
40
45
50
55
60
65
70
Canary rockfish n=105
0.40 0.35
0.20
0.30 0.15
0.25 0.20
0.10
0.15 0.10
0.05
0.05 0.00
20 25 30 35 40 45 50 55 60 65 70 75 80
Size class (cm)
0.00
10
15
20
25
30
35
40
45
Size class (cm)
Fig. 3. Size distribution (total length, cm) of six representative species (species that are harvested, have adequate sample sizes, and are either mostly mature or mostly immature). Sizes were binned into 5-cm classes. Dotted line indicates length at first maturity. n ¼ total number.
combination of boulder, cobble, and brachiopods correlated best with the transect species patterns. The single habitat that best matched the transect species patterns was boulder (r ¼ 0.63). 4. Discussion An occupied submersible proved to be an effective tool to survey demersal habitats and assemblages of fishes on the continental shelf off central California. This tool provided detailed in situ viewing by observers and additional viewing from the associated video images. The combined use of the observer and the video tape resulted in higher accuracy of fish identification and enumeration. From within the submersible, observers were able to identify small species (Yoklavich and O’Connell, 2008; Love et al., 2009), many of which would not have been identifiable by the video tape alone (i.e., produced from remotely operated vehicles or tow cameras). Despite the high diversity and numbers of small fishes occurring in
our study site, we were able to identify a large percentage of them to species using this tool. Total fish densities in this study were somewhat similar to those estimated using the same submersible in similar habitats and depths elsewhere along the Pacific shelf. Stein et al. (1992) reported an average density of 0.3 fish m2 in boulder habitat and 0.2 fish m2 in mud in surveys off Oregon, while densities in this study were 0.2 fish m2 in both boulder and mud habitats. In southern Monterey Bay, Anderson and Yoklavich (2007) reported higher densities (1.4 fish m2) in high relief rock, but similar density in low relief sediments (0.1 fish m2). Love and Schroeder (2007), surveying high relief, rocky outcrops in southern California, reported densities for all species combined at about 2 fish m2, with squarespot rockfish accounting for a minimum of 78% of all fish. It may be that rocky substrata in northern areas (including the Davenport shelf) are less productive than areas to the south or that rockfish densities are high around high relief as compared to the
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637 Table 4 Habitat selectivity index for 34 species (or species groups) that comprised at least 5% of the total abundance on a single transect. A positive index indicates the species was more abundant than randomly expected and a negative value indicates that species abundance was lower than randomly expected in each of the 4 primary habitats. Bolded text identifies those species having distributions not significantly different from random (P > 0.05). Species
Boulder
Brachiopod
Cobble
Mud
Blackeye goby Bocaccio Calico rockfish Canary rockfish Dover sole English sole Flatfish (unidentified) Greenspotted rockfish Greenstriped rockfish Hagfish (unidentified) Halfbanded rockfish Icelinid sculpin Kelp greenling Lingcod Petrale sole Pink seaperch Poacher (unidentified) Pygmy rockfish Rex sole Rock sole Ronquil Rosy rockfish Sanddab (unidentified) Sculpin (unidentified) Sebastomus (unidentified) Shortspine combfish Squarespot rockfish Starry rockfish Stripetail Threadfin sculpin Vermilion rockfish Widow rockfish Yellowtail rockfish YOY rockfish
23.1 56.7 12.5 50.4 20.5 32.0 28.9 0.9 23.7 18.7 10.1 33.0 25.1 19.0 33.0 2.4 32.5 54.3 33.0 21.9 49.3 50.7 32.5 11.6 29.5 7.6 54.2 57.4 20.5 33.0 42.6 15.0 47.5 39.1
7.5 8.0 8.0 8.0 4.5 6.1 2.8 2.0 14.2 34.9 1.2 8.0 1.0 5.7 8.0 5.5 6.4 7.9 8.0 29.0 3.8 7.8 8.0 4.4 6.2 3.9 8.0 7.2 29.5 8.0 6.8 8.0 7.9 7.8
0.1 6.0 12.2 6.0 6.0 5.0 3.0 2.0 0.4 6.0 31.4 12.2 6.0 2.6 6.0 4.1 6.0 1.0 6.0 1.4 6.0 0.7 5.0 4.7 7.8 11.9 0.1 3.9 6.5 6.0 4.8 6.0 1.1 0.4
15.8 42.7 16.6 36.4 22.0 43.1 34.7 4.9 10.0 10.1 22.5 28.8 18.1 22.1 47.0 12.0 44.8 47.4 47.0 8.6 39.5 43.6 45.5 11.3 31.0 8.2 8.0 46.3 15.5 47.0 31.0 1.0 38.6 31.8
relatively low relief boulder habitat in our study. Fish densities in our study were similar to those in a nearby deepwater canyon (>100 m depth; 0.2 fish m2) (Yoklavich et al., 2000), while fish densities from waters deeper than 100 m off Big Creek Marine Reserve (a remote area off central California that has received relatively little fishing) were somewhat higher ranging from 0.3 to 0.5 fish m2 (Yoklavich et al., 2002). The most common species, pygmy rockfish and blackeye gobies, also are abundant in other locations on the continental shelf. These two species have similar distributions from Canada to Baja California (Eschmeyer et al., 1983; Love et al., 2002). Pygmy rockfish were the most abundant species occurring on rock habitat in southern Monterey Bay, California (Anderson and Yoklavich, 2007), and on Heceta Bank, Oregon (Stein et al., 1992). Pygmy rockfish also were abundant at Big Creek Ecological Reserve in central California (Yoklavich et al., 2002), but not nearly as abundant as in the two other studies. The distribution of pygmy rockfish also extended to deeper depths (>100 m), where it was found to be the third most abundant species off Big Creek (Yoklavich et al., 2002) and twelfth most abundant in a submarine canyon in Monterey Bay (Yoklavich et al., 2000). Blackeye gobies were abundant in surveys from similar depths (Yoklavich et al., 2002; Love et al., 2006; Anderson and Yoklavich, 2007), and were the third most abundant fish species on rocky outcrops in southern California between the depths of 45–50 m (Love and Schroeder, 2007). Blackeye gobies were present, but scarce, in depths >100 m in Monterey Bay (Yoklavich et al., 2000). No mention of blackeye gobies was made from surveys off
635
Table 5 Species that characterize the 15 statistically significant groups of transects (P < 5%). Also indicated are: number of transects (n); the average similarity between all pairs of transects within each group; mean similarity between transects/standard deviation (SD), a measure of the consistency with which a species contributes to the similarity within transects (high value ¼ consistent presence of a species); the percent contribution of a species to the overall similarity of the transects within a group. The most abundant habitat for each group is also indicated to help with interpretation of the species groups. Species
Mean similarity/SD
%Contribution
Group f (n ¼ 2, ave. similarity ¼ 78%, Boulder habitat) Pygmy rockfish * Greenstriped rockfish * Greenspotted rockfish * Lingcod * Bocaccio * Rosy rockfish * Flatfish (unidentified) * Rockfish (unidentified) * Starry rockfish * Sebastomus spp. *
21.6 11.3 10.4 8.7 8.3 7.7 7.2 7.0 6.1 6.1
Group i (n ¼ 13, ave. similarity ¼ 72%, Boulder habitat) Pygmy rockfish 5.7 Yellowtail rockfish 6.4 Rosy rockfish 5.8 Sebastomus spp. 9.5 Blackeye goby 4.4 Rockfish (unidentified) 2.0 Starry rockfish 2.3 Squarespot rockfish 1.3
19.0 11.9 11.6 10.9 10.5 7.8 7.4 6.5
Group c (n ¼ 2, ave. similarity ¼ 71%, Boulder habitat) Blackeye goby * Rosy rockfish * Sebastomus spp. * Yellowtail rockfish * Flatfish (unidentified) * Kelp greenling * Rockfish (unidentified) * Sculpin (unidentified) *
17.2 14.8 12.4 11.3 9.5 9.5 9.5 8.0
Group d (n ¼ 6, ave. similarity ¼ 77%, Boulder habitat) Blackeye goby 10.9 Rosy rockfish 12.4 Northern ronquil 6.3 Yellowtail rockfish 14.2 Flatfish (unidentified) 11.1 Lingcod 10.5 Starry rockfish 5.7 Sanddab (unidentified) 1.3 Sebastomus spp. 1.4 Rockfish (unidentified) 1.4
16.4 14.3 10.2 9.7 8.1 7.7 6.6 5.9 4.8 4.7
Group g (n ¼ 2, ave. similarity ¼ 76%, Boulder habitat) Blackeye goby * Rockfish (unidentified) * Rosy rockfish * Sebastomus spp. * Greenspotted rockfish * Starry rockfish *
20.0 17.9 17.8 14.1 11.2 9.6
Group j (n ¼ 4, ave. similarity ¼ 76%, Boulder habitat) Rosy rockfish 30.6 Blackeye goby 5.7 Yellowtail rockfish 8.6 Starry rockfish 9.4 Rockfish (unidentified) 12.5 Sebastomus spp. 12.5 Greenspotted rockfish 15.0 Vermilion rockfish 6.8 Bocaccio 3.6
12.7 12.7 12.5 9.8 9.2 8.9 7.3 7.3 7.0
Group e (n ¼ 2, ave. similarity ¼ 69%, Mud/Boulder habitat) Rosy rockfish *
15.0
(continued on next page)
636
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
Table 5 (continued )
Table 5 (continued )
Species
Mean similarity/SD
%Contribution
Species
Sanddab (unidentified) Blackeye goby Pink surfperch Starry rockfish Flatfish (unidentified) Yellowtail rockfish Canary rockfish Rockfish (unidentified)
* * * * * * * *
13.4 13.1 9.8 9.5 9.1 8.5 7.2 7.2
Group m (n ¼ 4, ave. similarity ¼ 64%, Mud/Cobble habitat) Greenstriped rockfish 4.4 Greenspotted rockfish 4.4 Flatfish (unidentified) 2.9 Sanddab (unidentified) 3.9 Sebastomus spp. 7.4 Sculpin (Icelinus spp.) 9.4 Sculpin (unidentified) 6.5
Group k (n ¼ 24, ave. similarity ¼ 70%, Mud/Boulder habitat) Blackeye goby 4.8 Rosy rockfish 5.0 Yellowtail rockfish 5.8 Greenspotted rockfish 5.3 Sebastomus spp. 2.7 Rockfish (unidentified) 2.1 Starry rockfish 2.2 Lingcod 2.1 Greenstriped rockfish 1.7
13.7 10.7 10.5 10.5 8.6 7.4 6.4 6.3 6.3
Group o (n ¼ 10, ave. similarity ¼ 68%, Mud/Boulder habitat) Blackeye goby 9.0 Greenspotted rockfish 10.4 Greenstriped rockfish 4.6 Flatfish (unidentified) 7.6 Rosy rockfish 1.9 Pink surfperch 1.3 English sole 1.3
16.6 14.3 11.5 10.7 9.3 6.2 5.5
Group b (n ¼ 2, ave. similarity ¼ 87%, Mud habitat) Flatfish (unidentified) * Poacher (unidentified) * Sanddab (unidentified) * Greenstriped rockfish * Rex sole * English sole *
20.4 20.3 17.8 15.5 13.0 13.0
Group n (n ¼ 3, ave. similarity ¼ 69%, Mud habitat) Greenstriped rockfish 29.4 Greenspotted rockfish 5.6 Flatfish (unidentified) 10.2 English sole 4.4 Lingcod 12.4 Poacher (unidentified) 5.9 Sebastomus spp. 15.1 Rock sole 73.8
18.5 12.4 12.3 9.5 9.3 9.1 8.8 8.5
Group p (n ¼ 19, ave. similarity ¼ 69%, Mud habitat) Flatfish (unidentified) 6.3 Sanddab (unidentified) 7.3 Poacher (unidentified) 5.5 Greenstriped rockfish 2.6 English sole 1.8 Blackeye goby 1.9 Greenspotted rockfish 1.8 Pink surfperch 1.5
15.4 14.6 14.1 10.8 10.2 10.1 9.5 8.6
Group l (n ¼ 6, ave. similarity ¼ 60%, Greenstriped rockfish Flatfish (unidentified) Greenspotted rockfish Lingcod Pink surfperch
24.5 19.7 19.1 11.0 9.2
Oregon (Pearcy et al., 1989; Stein et al., 1992), which were in slightly deeper water and may be below the depth range of this species in the north. These data indicate that pygmy rockfish and blackeye gobies are abundant throughout much of their range. Utilization of brachiopod beds as a fish habitat has not been reported prior to this study. Brachiopods occur in a turbid area of the continental shelf on a thin mud bottom, attaching themselves to both living and dead conspecifics (Pennington et al., 1999). This habitat type had the lowest abundance and diversity of fishes, and only two species (greenspotted and greenstriped rockfishes) were commonly observed in and around brachiopods; a few other species, such as small flatfishes and lingcod also were occasionally seen. It may be that brachiopod beds are not associated with suitable prey or perhaps the beds are an ephemeral habitat that is periodically covered by the surrounding sediment and not consistently available as shelter for these fishes. Fishes less than 20 cm accounted for over 80% of all fish observed during our survey. Most of the large species (>25 cm as adults) were represented by small, immature individuals. This occurred across species groups, including rockfishes, flatfishes, and lingcod. The absence of large fishes was not unique to this area. Love et al. (2006) found most individuals of vermilion, flag (S. rubrivinctus), and greenspotted rockfishes were immature during a survey off southern California in waters from 75–79 m deep. In a study on the southern side of Monterey Bay, Anderson and Yoklavich (2007) observed more small (<20 cm) commercially important species than larger individuals. Yoklavich et al. (2000) reported that most greenspotted rockfish were immature from areas <175 m; however, at deeper depths most of the rockfishes were mature. Yoklavich et al. (2002) reported that young-of-theyear rockfishes accounted for 30–82% of the total fish surveyed in water depths <100 m, but represented only 0.7–1.9% of the total fish counted in water depths >100 m. The abundance of immature fishes may indicate that this area of the shelf is a nursery for younger fishes. In a study off Oregon, Pearcy et al. (1989) suggested that a nursery ground for young rockfishes was located on the top of the offshore Heceta Bank (100 m). Love and Schroeder (2007) reported relatively few large individuals of large species on rocky outcrops from 45–50 m water depth, and suggested that larger individuals migrated to deeper water. Many fish species exhibit ontogenetic habitat shifts (Hallacher and Roberts, 1985; Johnson et al., 2001; Love et al., 2006; Love and Yoklavich, 2008). Auster et al. (2003) observed juvenile Acadian redfish (Sebastes fasciatus) on Stellwagen Bank in different habitats than the adults, leading the authors to surmise that the surveyed area could be a recruitment habitat. Four flatfish species were found to have ontogenetic shifts in habitat (mainly in depth) in the Gulf of Maine (Methratta and Link, 2007). Juvenile pollock (Theragra chalcogramma) have been shown to live in shallow nursery areas off Japan and in the Bering Sea before moving to deeper adult habitats (Nishimura et al., 2007; Winter et al., 2007). The young of many species (rockfishes, lingcod, and flatfishes) recruit from the plankton to shallow areas and move deeper to adult habitat as they grow (Love et al., 2002). Our study site on the
Mud/Brachiopod habitat) 7.6 5.4 9.2 1.3 1.4
Group q (n ¼ 11, ave. similarity ¼ 64%, Mud/Brachiopod habitat) Greenspotted rockfish 5.4 Greenstriped rockfish 4.7 Lingcod 5.0 Blackeye goby 1.9 Sebastomus spp. 2.0 Shortspine combfish 2.0 Flatfish (unidentified) 1.3
17.1 16.4 12.0 11.7 8.8 8.2 7.4
Mean similarity/SD
%Contribution 16.0 14.4 11.6 11.6 11.5 10.1 10.0
T.E. Laidig et al. / Estuarine, Coastal and Shelf Science 83 (2009) 629–637
shelf may be an intermediate staging area between the shallow, nearshore young-of-the-year habitats and deeper, adult habitats. It also is possible that the lack of mature fishes is due to past fishing pressure and that populations in this area have not yet recovered. The study area has been closed to recreational fishing and has received limited commercial fishing since 2002 (PFMC, 2003). Prior to that time, this area had been fished heavily by both commercial trawl and longline gear as well as recreational fishermen for at least 100 years. Baskett et al. (2006) suggested that, in areas where large predatory fishes were removed and small species dominate, stock recovery of the larger species may be slowed due to competition for food and shelter resources between the juveniles of the once dominant larger species and the small-sized species. Unfortunately, no prior visual survey data are available from this area, and comparison with commercial and recreational catches would under-represent the small fishes that were so prevalent in our study. This study provides post-fishery baseline data and additional visual surveys will be needed to monitor the potential recovery of this shelf assemblage as time of protection increases. These additional surveys will be invaluable in determining whether these habitats can support populations of mature fishes. Relatively few habitat surveys have focused on the intermediate depths (30–100 m) of the continental shelf off the west coast of the United States. This area may be an important nursery ground and may replenish deeper areas with maturing fishes. Knowledge of the fish and habitat associations at different life stages is critical in determining the placement of marine protected areas and in rebuilding stocks. Any ecosystem-based management objectives should consider vital areas such as this study site. Using fish–habitat associations, combined with broad-scale seafloor habitat maps, could improve our groundfish stock assessments for several species. Acknowledgments We thank the crews of the R/V Velero IV and the Delta submersible for their fine work during this study. We also thank Linda Snook and John Field for help with submersible observations, and Lisa Wooninck and Zoe Schumacher for logistical help during the cruise. We thank E.J. Dick for help in statistical matters, and S. Sogard, J. Mason, and K. Sakuma for their comments on earlier drafts of the manuscript. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.ecss.2009.05.008. References Anderson, T.J., Yoklavich, M.M., 2007. Multi-scale habitat associations of deep-water demersal fishes off central California. Fishery Bulletin 105, 168–179. Auster, P.J., Lindholm, J., Valentine, P.C., 2003. Variation in habitat use by juvenile Acadian redfish, Sebastes fasciatus. Environmental Biology of Fishes 68, 381–389. Baskett, M.L., Yoklavich, M., Love, M.S., 2006. Predation, competition, and the recovery of exploited fish stocks in marine reserves. Canadian Journal of Fish and Aquatic Science 63, 1214–1229. Bray, J.R., Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27, 325–349. Carr, M.H., 1991. Habitat selection and recruitment of an assemblage of temperate zone reef fishes. Journal of Experimental Marine Biology and Ecology 146, 113–137. Christensen, V., Guenette, S., Heymans, J.J., Walters, C.J., Watson, R., Zeller, D., Pauly, D., 2003. Hundred-year decline of North Atlantic predatory fishes. Fish and Fisheries 4, 1–24. Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK, 91 pp. Cormack, R.M., 1971. A review of classification. Journal of the Royal Statistical Society Series A 134, 321–367.
637
DeMartini, E.E., Roberts, D.A., 1990. Effects of giant kelp (Macrocystis) on the density and abundance of fish in a cobble-bottom kelp forest. Bulletin of Marine Science 46, 287–300. Echeverria, T.W., 1987. Thirty-four species of California rockfishes: maturity and seasonality of reproduction. Fishery Bulletin 85, 229–250. Eschmeyer, W.N., Herald, E.S., Hammann, H., 1983. Pacific Coast fishes. Houghton Mifflin, Co, Boston, MA, 336 pp. Eittreim, S.L., Anima, R.J., Stevenson, A.J., 2002. Seafloor geology of the Monterey Bay area continental shelf. Marine Geology 181, 3–34. Fishbase, 2007. Shortspine combfish Web Page. http://www.fishbase.org. Greene, H.G., Yoklavich, M.M., Starr, R.M., O’Connell, V.M., Wakefield, W.W., Sullivan, D.E., McRea, J.E., Cailliet, G.M., 1999. A classification scheme for deep seafloor habitats. Oceanologica Acta 22, 663–678. Hallacher, L.E., Roberts, D.A., 1985. Differential utilization of space and food by inshore rockfishes (Scorpaenidae: Sebastes) of Carmel Bay, California. Environmental Biology of Fishes 12, 91–110. Hart, J.L., 1973. Pacific Fishes of Canada. Fisheries Research Board of Canada, Ottawa, 740 pp. Johnson, K.A., Yoklavich, M.M., Cailliet, G.M., 2001. Recruitment of three species of juvenile rockfish (Sebastes spp.) on soft benthic habitat in Monterey Bay, California. CalCOFI Reports 42, 153–166. Laidig, T.E., Chess, J.R., Howard, D.F., 2007. Relationship between abundance of juvenile rockfishes (Sebastes spp.) and environmental variables documented off northern California and potential mechanisms for the covariation. Fishery Bulletin 105, 39–48. Love, M.S., 1996. Probably More than you Want to Know about the Fishes of the Pacific Coast. Really Big Press, Santa Barbara, CA, 381 pp. Love, M.S., Schroeder, D.M., 2007. A characterization of the fish assemblage of deep photic zone rock outcrops in the Anacapa Passage, southern California, 1995 to 2004, with evidence of a regime shift. CalCOFI Reports 48, 165–176. Love, M.S., Yoklavich, M.M., 2008. Habitat characteristics of juvenile cowcod, Sebastes levis (Scorpaenidae), in southern California. Environmental Biology of Fishes 82, 195–202. Love, M.S., Yoklavich, M., Thorsteinson, L., 2002. The Rockfishes of the Northeast Pacific. University of California Press, Berkeley and Los Angeles, CA, 405 pp. Love, M.S., Schroeder, D.M., Lenarz, B., Cochrane, G.R., 2006. Gimme shelter: the importance of crevices to some fish species inhabiting a deeper-water rocky outcrop in southern California. CalCOFI Reports 47, 119–126. Love, M.S., Yoklavich, M., Schroeder, D.M., 2009. Demersal fish assemblages in the southern California Bight based on visual surveys in deep water. Environmental Biology of Fishes 84, 55–68. Methratta, E.T., Link, J.S., 2007. Ontogenetic variation in habitat associations for four flatfish species in the Gulf of Maine-Georges Bank region. Journal of Fish Biology 70, 1669–1688. Nishimura, A., Hamatsu, T., Shida, O., Mihara, I., Mutoh, T., 2007. Interannual variability in hatching period and early growth of juvenile walleye Pollock, Theragra chalcogramma, in the Pacific coastal area of Hokkaido. Fisheries Oceanography 16, 229–239. Paddock, M.J., Estes, J.A., 2000. Kelp forest fish populations in marine reserves and adjacent exploited areas of central California. Ecological Applications 10, 855–870. Parker, S.J., Berkeley, S.A., Golden, J.T., Gunderson, D.R., Heifetz, J., Hixon, M.A., Larson, R., Leaman, B.M., Love, M.S., Musick, J.A., O’Connell, V.M., Ralston, S., Weeks, H.J., Yoklavich, M.M., 2000. Management of Pacific Rockfish. Fisheries 25, 22–29. Pearcy, W.G., Stein, D.L., Hixon, M.A., Pikitch, E.K., Barss, W.H., Starr, R.M., 1989. Submersible observations of deep-reef fishes of Heceta Bank, Oregon. Fishery Bulletin 87, 955–965. Pennington, J.T., Tamburri, M.N., Barry, J.P., 1999. Development, temperature tolerance, and settlement preference of embryos and larvae of the articulate brachiopod Laqueus californianus. Biological Bulletin 196, 245–256. PFMC (Pacific Fishery Management Council), 2003. Final environmental impact statement for the proposed groundfish acceptable biological catch and optimum yield specifications and management measures: 2003 Pacific Coast Groundfish Fishery, Portland OR, 206 pp. Phillips, J.B., 1964. Life history studies on ten species of rockfish (Genus Sebastodes). California Department of Fish and Game Fish Bulletin 126, 70 pp. Rothrock, G.C., 1973. Age-length, weight, fecundity, and meristics of the kelp greenling (Hexagrammos decagrammus) off California. M.S. Thesis, University of California, Davis, 95 pp. Stein, D.L., Tissot, B.N., Hixon, M.A., Barss, W., 1992. Fish–habitat associations on a deep reef at the edge of the Oregon continental shelf. Fishery Bulletin 90, 540–551. Winter, A., Coyle, K.O., Swartzman, G., 2007. Variations in age-0 pollock distribution among Bering Sea nursery areas: A comparative study through acoustic indices. Deep Sea Research (Part II, Topical Studies in Oceanography) 54, 2869–2884. Yoklavich, M.M., O’Connell, V., 2008. Twenty years of research on demersal communities using the Delta submersible in the northeast Pacific. In: Reynolds, J.R., Greene, H.G. (Eds.), Alaska Sea Grant College Program. University of Alaska Marine habitat mapping technology for Alaska, Fairbanks, pp. 143–155. Yoklavich, M.M., Greene, H.G., Cailliet, G.M., Sullivan, D.E., Lea, R.N., Love, M.S., 2000. Habitat association of deep-water rockfishes in a submarine canyon: an example of a natural refuge. Fishery Bulletin 98, 625–641. Yoklavich, M.M., Cailliet, G.M., Lea, R.N., Greene, H.G., Starr, R.M., de Marignac, J., Field, J., 2002. Deepwater habitat and fish resources associated with the Big Creek Marine Ecological Reserve. CalCOFI Reports 43, 120–140.