Bull Mar Sci. 95(4):657–681. 2019 research paper https://doi.org/10.5343/bms.2018.0009
Site fidelity, vertical movement, and habitat use of nearshore reef fishes on offshore petroleum platforms in southern California
1 California State University Long Carlos Mireles 1, 2 * Beach, Department of Biological Christopher JB Martin 1 Sciences, 1250 Bellflower Blvd., 1 Long Beach, California 90840. Christopher G Lowe 2 Current Address: California Department of Fish and Wildlife, 1933 Cliff Dr. Suite 9, Santa Barbara, California 93109. ABSTRACT.—Off California, economically important * Corresponding author emails: nearshore reef fishes inhabit the shallow (<20 m) regions of
The California Artificial Reef Program was created in 2010 as part of the California Marine Resources Legacy Act (Assembly Bill 2503), which authorizes the retention of offshore petroleum platform structures as artificial reef once extractive activities cease (Pietri et al. 2011). Many of California’s 27 offshore platforms have
Bulletin of Marine Science 657 © 2019 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 658 Bulletin of Marine Science. Vol 95, No 4. 2019 been operational for >40 yrs and are expected to end production in the near future (Schroeder and Love 2004, Claisse et al. 2015). Under Assembly Bill 2503, platforms will be evaluated to determine whether they “act as net resources to marine resources,” and may be eligible for reefing (Bernstein 2015). If deemed eligible for reefing, structures may be partially removed, whereby the upper portion of the platform to 26 m depth will be removed, leaving the remaining structure in place as habitat (Love et al. 2003, Claisse et al. 2015). Over the last 20 yrs, considerable effort has focused on quantifying the ecological importance of California offshore petroleum platforms, with a vast majority of that work addressing structural community metrics (e.g., diversity, fish density, biomass, species composition) of fishes and invertebrates in comparison to natural reefs (Love et al. 1999, 2000, Caselle et al. 2002, Love and York 2005, 2006, Emery et al. 2006, Page et al. 2007, Martin and Lowe 2010). Extensive invertebrate communities colonize the upper reaches of platform jackets, providing considerable food resources for associated fish communities (Bram et al. 2005, Page et al. 2007, 2008, Martin et al. 2012). Because of the depth of many platforms off California, human submersible surveys have been the primary method of assessing fish community structure and abundance from the surface to the seafloor (Love et al. 1999, 2000, Love and York 2005, 2006); however, due to the costs and logistical constraints of these types of surveys, platforms were often surveyed only once per year and allowed only for counts of fish seen from the outside of each platform (Claisse et al. 2014, Pondella et al. 2015). Diver-based visual surveys have also been conducted for shallower platforms (those shallower than 30 m) or only the upper reaches (<30 m) of deeper platforms, which allowed for observations of fishes inside the platform structure and across multiple seasons (Carr et al. 2003, Love et al. 2003, Martin and Lowe 2010). Fish surveys have shown that assemblages associated with offshore petroleum platforms vary across their range in southern California, with cold temperate species typical of the Oregonian Province (Horn et al. 2006) primarily inhabiting northern platforms in the Santa Maria Basin (SMB) and western Santa Barbara Channel (SBC; Love et al. 1999, 2000, 2003), and warm temperate species commonly associated with the San Diegan province (Horn et al. 2006) inhabiting eastern SBC platforms (Carlisle et al. 1964, Carr et al. 2003, Love et al. 2003) and southern San Pedro Shelf (SPS) platforms (Love et al. 2003, Martin and Lowe 2010). In addition, fish assemblages throughout the region vary by depth of platforms. The vertical orientation of offshore petroleum platforms offers continuous habitat from the benthos to the surface, much like a rock pinnacle, allowing for more diverse fish assemblages with seasonal variation and depth stratification (Carlisle et al. 1964, Carr et al. 2003, Love et al. 1999, 2003, Martin and Lowe 2010). Aspects of habitat created by offshore petroleum platforms, such as shading, horizontal and vertical substratum, and encrusting invertebrates, are important to the ecology of natural and artificial nearshore reefs (Bohnsack and Sutherland 1985, Sonu and Grove 1985, Grove et al. 1989, Martin et al. 2012). For example, fishes have been observed to use crevices formed between the benthos and horizontal cross beams, as well as between the benthos and connecting pipelines (Love and York 2005, 2006). In addition, operational debris along the seafloor (Caselle et al. 2002), mussel shell mounds at the base of platforms (Wolfson et al. 1979, Love et al. 1999), and horizontal levels characterized by a network of horizontal cross beams that provide structural support (Carlisle et al. 1964, Carr et Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 659 al. 2003, Love et al. 2003, Martin and Lowe 2010), have all been shown to provide refuge habitat for various life stages of economically important fish species. Based on structural metrics of fish communities associated with California offshore petroleum platforms, these artificial structures have been argued to be some of the most productive marine habitats in the world (Claisse et al. 2014, Pondella et al. 2015). However, estimation of standing stock productivity and composition based on static measures of platform-associated fish populations alone do not directly quantify the ecological benefit of these structures for regional fish populations. To better quantify the ecological benefits of offshore petroleum platforms for fish assemblages, it is important to consider functional metrics, including trophic connectivity, degrees of site fidelity to estimate the residency times of individuals, and mating and spawning activity. Many of these functional metrics require understanding the behavior of individuals and how they use platform structures during their times of residency. Lowe et al. (2009) used passive acoustic telemetry monitoring to quantify the site fidelity of 17 species of deeper reef fishes to platforms in the western SBC over a 1.5-yr period and found high intra- and interspecific variability. In addition, some individuals emigrated from shallower platforms to deeper ones, while others moved between platforms and natural habitats (Lowe et al. 2009). Another acoustic telemetry monitoring study in the SBC found that demersal rockfishes, Sebastes spp., and lingcod, Ophiodon elongatus Girard, 1854, homed back to their original platform after being translocated to natural reefs up to 19 km away (Anthony et al. 2013). Twenty-seven percent of vermilion rockfish, Sebastes miniatus (Jordan and Gilbert, 1880), translocated from platforms homed back to platforms, suggesting that some individuals may choose to reside at platform habitat over natural habitat (Anthony et al. 2013). These studies were primarily focused on cold temperate fish species associated with the mid-water and bottom portions of western SBC platforms; however, no studies to date have examined the site fidelity of nearshore reef fish occupying platforms on the SPS, which consist of both warm and cold temperate species. In addition, no study has yet examined the depth distribution and habitat use of nearshore reef fishes on any California offshore platform over an extended period of time. Under a partial removal strategy, as permitted under Assembly Bill 2503, the shallowest portion of the platform structure (<26 m) would be removed. However, these shallow portions are where the predominant nearshore reef fish species have been noted to occur at SPS petroleum platforms (Carr et al. 2003, Love et al. 2003, Martin and Lowe 2010), many of which have been found to display high degrees of site fidelity to natural reef (Hartmann 1987, Lowe et al. 2003, Topping et al. 2006, Freiwald 2012, Mireles et al. 2012). At deeper SPS platforms, such as Eureka, the seafloor depth (212 m) is greater than the documented depth range of many of the species inhabiting the shallow regions of the platform (Love 1996, Eschmeyer and Herald 1999). Given the dominance of warm temperate nearshore reef fishes at SPS platforms (Martin and Lowe 2010), it is unknown to what extent these species utilize deeper platform habitat, their overall site fidelity, and whether these behaviors are influenced by platform depth. This understanding is critical to determine the ecological importance of these shallow portions of platform habitat to these species and to assess how populations may be influenced by various decommissioning options. The goals of the present study were to: (1) quantify the long-term, seasonal, and daily site fidelity of cabezon, Scorpaenichthys marmoratus (Ayres, 1854), grass 660 Bulletin of Marine Science. Vol 95, No 4. 2019 rockfish, Sebastes rastrelliger (Jordan and Gilbert, 1880), kelp rockfish, Sebastes atrovirens (Jordan and Gilbert, 1880), and California sheephead, Semicossyphus pulcher (Ayres, 1854) at one shallow (50 m bottom depth) and one deep (212 m bottom depth) offshore petroleum platform on the SPS for 1.5 yrs; (2) determine the depth and habitat use of a subsample of these individuals over a 1-yr period; and (3) assess the conservation value of the various decommissioning options in the context of fisheries resource management.
Materials and Methods
Study Sites Passive acoustic telemetry was used to monitor fish at two offshore petroleum plat- forms located approximately 13 km off the coast of Huntington Beach, California, on the SPS, from 18 June, 2007, through 15 January, 2009 (Fig. 1). Fish were tagged at platforms Edith (installed 1983; 50 m bottom depth) and Eureka (installed 1984; 212 m bottom depth), which are approximately 4 km apart. Extensive horizontal levels occur at two depths at platform Edith (about 15 and 30 m) and at nine depths at platform Eureka (approximately 17, 35, 60, 78, 99, 120, 140, 164, and 188 m). Two ad- ditional platforms, Ellen and Elly (80 and 77 m bottom depths, respectively), located equidistant between Edith and Eureka, were also outfitted with acoustic receivers to quantify possible interplatform movement. All platforms are located in mud/sand substratum, with nearest rock reef habitats located approximately 1 km to the west of platform Edith (150 Kelp Reef, 50 m depth), and approximately 2 km to the west of platform Eureka (SE Bank, 90 m depth). Horseshoe Reef is the nearest relatively shallow (20–30 m depth) natural rock reef habitat located approximately 12 km to the northwest of platform Edith. Fish Capture and Acoustic Tag Implantation Four economically important nearshore reef species, cabezon, California sheephead (herein sheephead), grass rockfish, and kelp rockfish, were captured using dipnets and diver held handlines rigged with baited hooks at platforms Edith and Eureka. Fish were targeted from 15 to 30 m depth. Once captured, individuals were placed in a mesh bag and brought to the surface for tagging. At the surface, fish were placed in a chilled seawater bath dosed with clove oil (30 mg L−1) until sedated. Initially, 10 fish of each species (five from each platform) were surgically fitted with a uniquely coded acoustic transmitter (Vemco Ltd. V13-1L-R64K, frequency 69 kHz, power output 147 dB, nominal battery life 800 d, 13 mm diameter × 36 mm long, pulse interval 100– 300 s). An additional five individuals of each species were fitted with depth-sensing coded transmitters (Vemco Ltd. V13P-1L-S256, frequency 69 kHz, power output 147 dB, nominal battery life 518 d, 13 mm diameter × 45 mm long, pulse interval 30–90 s, max depth 204 m, pressure sensor resolution 0.9 m, accuracy ±1.7 m at 17 m depth, ±10 m at 204 m depth). After it was determined that three tagged individuals were not detected after release, one additional kelp rockfish and one sheephead were fitted with a V13-1L-R64K transmitter, with one additional sheephead fitted with a V13P- 1L-S256 transmitter, for a total of 63 tagged individuals (Table 1). A small, 1-cm long incision was made through the abdominal wall along the mid- line between the pelvic fins and anal pore, and a transmitter was inserted into the peritoneal cavity. Prior to implantation, transmitters were coated with a beeswax Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 661
Figure 1. (A) Distribution of all 27 California petroleum platforms (black points). (B) Platforms on the San Pedro Shelf, including study platforms Edith, Ellen, Elly, and Eureka (encircled). Bathymetry lines represent 10 m isobaths.
Table 1. Initial tagging summary of cabezon (Scorpaenichthys marmoratus), grass rockfish (Sebastes rastrelliger), kelp rockfish (Sebastes atrovirens), and California sheephead (Semicossyphus pulcher) individuals by platform.
Capture depth (m) Species/ Total Mean total length Tagging Tagging Platform tagged (SE), cm Minimum Maximum start date completion date Cabezon Edith 8 40.4 (3.2) 15 30 30 Jun, 2007 27 Oct, 2007 Eureka 7 35.1 (1.3) 17 30 18 Jun, 2007 22 Jul, 2007 Total 15 37.9 (1.9) 15 30 18 Jun, 2007 27 Oct, 2007 Grass rockfish Edith 7 35.8 (1.2) 15 20 23 Jun, 2007 9 Aug, 2007 Eureka 8 33.0 (1.1) 17 20 25 Jun, 2007 16 Jul, 2007 Total 15 34.3 (0.9) 15 20 23 Jun, 2007 09 Aug, 2007 Kelp rockfish Edith 7 33.2 (1.5) 15 25 23 Jun, 2007 4 Nov, 2007 Eureka 9 32.5 (0.4) 18 25 21 Jun, 2007 15 Dec, 2007 Total 16 32.8 (0.7) 15 25 21 Jun, 2007 15 Dec, 2007 Sheephead Edith 8 53.2 (2.4) 15 17 23 Jun, 2007 18 Jul, 2007 Eureka 9 49.1 (2.0) 15 17 18 Jun, 2007 27 Oct, 2007 Total 17 51.0 (1.6) 15 17 18 Jun, 2007 27 Oct, 2007 All species Total 63 39.3 (1.2) 15 30 18 Jun, 2007 15 Dec, 2007 662 Bulletin of Marine Science. Vol 95, No 4. 2019 and paraffin mixture (1:2.3) to decrease the probability of immunorejection (Lowe et al. 2003, Topping et al. 2005). The incision wound was closed using two interrupted sutures of Ethicon Chromic Gut. All fish were measured for total length (TL) and were revived in fresh seawater, and externally tagged with a serial coded spaghetti nylon dart type tag (Hallprint, 7.5 cm length). External tags were color coded by plat- form so that fish could be identified during corresponding dive surveys (Martin and Lowe 2010). The entire tagging procedure took <10 mins. All fish capture, handling, and surgical procedures were approved under the California State University Long Beach Institutional Animal Care and Use Committee protocol #243. After tagging, revived fish were released at their site of capture by divers or placed in an upside-down weighted milk crate and lowered to the individual’s depth of capture as close to the platform as possible. Previous studies on these species indi- cated high postrelease survivorship using these procedures (Lowe et al. 2003, 2009, Topping et al. 2006, Anthony et al. 2013). Automated Acoustic Monitoring Prior to tagging fish at SPS platforms, a series of test were performed to character- ize the acoustic environment of the study platforms and determine the performance of acoustic receivers in the study setting. Background noise tests were performed over a 20-d period in March 2007 at each of the four monitored platforms to quantify the level of background noise present in absence of acoustic transmitters. No false positive detections were recorded during background noise tests; however, acoustic signals were detected by all receivers that resonated or had harmonics at the same operational frequency as acoustic transmitters used in our study (69 kHz). Range tests and detection efficiency tests were performed to determine the detection dis- tance of receivers and the capability of receivers to detect a transmitter that was placed at 12 known locations throughout platform Edith by scuba divers, which was replicated at 10, 15, and 30 m depths. Mean horizontal detection ranges for receivers located within all four platforms were 81 (SD 61.0) m, with mooring line receivers located adjacent to each platform displaying detection ranges of 498 (SD 31.1) m. Overall, detection efficiencies were 42% and 55% for receivers placed within platform Edith at 15 and 25 m, respectively, with the adjacent mooring line receiver (20 m depth) displaying a 19.4% detection efficiency. Sixty-seven percent of all transmitter signals occurring between 10 and 30 m were detected by either the shallow (15 m) or deep (25 m) platform receiver. This suggested that the placement of the receiv- ers at these depths provided relatively strong acoustic coverage within the platform between 10 and 30 m depths, while also suggesting that 33% of detections would go undetected. Detection range and detection efficiency tests were found to be most influenced by the platform structure itself posing a structural acoustic obstacle that prevented transmitter signals from reaching acoustic receivers positioned inside and outside the platform structures. To increase our capability of detecting an in- dividual while residing at platforms, acoustic receivers were added to areas where known acoustic shadows were present. Receivers were placed at 15 and 25 m depths to provide coverage above and below the typical depths of a thermocline to reduce potential thermocline effects on detection performance as described in Westmeyer et al. (2007). Findings from these tests were used to design a monitoring array that provided optimal coverage to record the daily presence and vertical movements of tagged individuals across multiple seasons. Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 663
Three automated omni-directional acoustic receivers (Vemco VR2W-69kHz) were suspended on short moorings within platform Eureka at depths of 15, 20, and 25 m. At platforms Edith, Ellen, and Elly, receivers were placed at 15 and 25 m within the platform structure. An additional receiver was placed on the vessel support mooring cable of platform Eureka and Edith (approximately 100 m from platform) at a depth of 20 m. VR2W acoustic receivers recorded the date, time, tag depth reading, and serial number of coded acoustic transmitters within detection range. Receivers were retrieved bimonthly, downloaded, and then redeployed. Receivers were removed from platform Edith on 14 January, 2009, after monitoring for 577 total days and platform Eureka on 15 January, 2009, after 578 total days. Environmental Conditions At platform Edith, water temperature and light data loggers (Hobo Pendant, 64K, model UA-002-64, temperature sensitivity ±0.47 °C at 25 °C) were placed every 5 m from the surface down to 30 m along the platform jacket and recorded data every 30 min. These data were used to characterize the temperature profile of the study -en vironment and to measure changes in the depth of the thermocline over the course of the study. Data Analysis Site Fidelity.—Based on the high levels of ambient noise detected during back- ground noise tests, it was determined that a conservative detection criterion was required. Therefore, a tagged individual was considered present at a platform only if it was detected at least three times in a given day. Fish were considered to have emi- grated from platforms, or possibly died, if they displayed consistent detection behav- ior for at least 10 d before detections ceased completely for an individual. Because the tagging procedure could lead to possible changes in behavior, including immediate emigration or death, only individuals detected for at least 10 d following tagging were used for site fidelity analyses. Three different measures were developed to quantify the site fidelity of tagged individuals over long-term, seasonal, and daily periods. Long-term site fidelity was measured by determining the proportion of individuals that were still detected at platforms during the last 2 wks of the study (1–15 January, 2009). Daily site fidelity was measured by determining the percentage of days that individuals were detected at a platform out of the total days that they were at liberty. For most individuals (68%), the last day of the study (15 January, 2009) was used as an end date. For indi- viduals with depth-sensing transmitters, the estimated expiration date for battery life was used as the end date if prior to 15 January, 2009. Long-term site fidelity values of each species were compared between platforms using a chi-square goodness of fit test (Sigmaplot 11.0, Systat Software, Inc.). Comparisons of each species daily site fi- delity values were made between platforms using a Mann-Whitney U test (Sigmaplot 11.0, Systat Software, Inc.). Seasonal daily site fidelity was quantified by determining the percentage of days that each individual was detected during fall (1 September–30 November, 2007), winter (1 December, 2007–29 February, 2008), spring (1 March–31 May, 2008), and summer (1 June–31 August, 2008). Only individuals that were de- tected at least one day during each of the seasons being compared were included in the comparative analysis. Comparisons of these seasonal daily site fidelity val- ues were made among seasons within each species using a Mann-Whitney U test (Sigmaplot 11.0, Systat Software, Inc). Nonparametric tests were required for all site 664 Bulletin of Marine Science. Vol 95, No 4. 2019 fidelity and depth comparative analysis due to these data not meeting the assump- tion of normal distribution. Attempts to transform data to meet assumptions of nor- mality were not successful due to the highly skewed nature of these data. Depth Distribution, Habitat Use, and Temperature Effect.—Seasonal daily depth use was analyzed by comparing the mean daily depth recorded for each species dur- ing each season as defined by fall 2007 (1 September–30 November, 2007), winter 2008 (1 December, 2007–29 February, 2008), spring 2008 (1 March–31 May, 2008), and summer 2008 (1 June–31 August, 2008) using a Kruskall-Wallis rank sums test, followed by a Dunn’s post hoc pairwise test to determine group differences (Sigmaplot 11.0, Systat Software, Inc.). For this analysis, the mean daily depths of each individual of the same species were combined to provide a population level mean of seasonal depth distribution. To determine the degree to which fish utilize horizontal support structures, the percentage of total depth detections that occurred at each horizon- tal level (the area 3 m above and below each level) and interhorizontal level areas at both platforms was quantified. The 3 m depth variance around each horizontal level was used to account for changes in tidal range and depth sensor resolution (±0.9 m). This was determined for all horizontal levels and interhorizontal spaces pooled, as well as for each depth specific horizontal level and interhorizontal level depth area. To determine the influence of water temperature on vertical movement and habitat use of individuals, the mean daily depths of cabezon, grass rockfish, and kelp rockfish, and the mean daytime depths (09:00–16:59) of sheephead were analyzed in relation to the strength of the thermocline (mean daily water temperature difference between 5 and 30 m) for the dates between 1 September, 2007, and 31 August, 2008, using a Kruskall-Wallis rank sums test, followed by a Dunn’s post hoc pairwise test to determine group differences (Sigmaplot 11.0, Systat Software, Inc.). Sheephead’s mean daytime depths were used for this comparison due to findings that individuals at both platforms exhibited sedentary behavior during night periods and increased vertical movement during daytime periods (C Mireles, California State University Long Beach, unpubl data).
Results
A total of 63 fish were tagged between 17 June and 15 December, 2007 (Table 1). Tagged individuals were monitored from 397 to 578 d, depending on when individu- als were originally released. Two grass rockfish (ID# 2985 and 190), four kelp rockfish (ID# 192, 2995, 2996, and 2987), and two sheephead (ID# 183 and 2983) were not included in any site fidelity analyses since they were either detected for a total of <10 d after being tagged or for individuals fitted with pressure sensing transmitters (i.e., ID# 192 and 183), did not display changes in vertical movement indicative of a live individual (Fig. 2). A total of 4.5 million detections were recorded from tagged individuals over the duration of the study. One cabezon (ID# 2994) was reported as being recaptured twice at platform Edith by recreational fishers. The first recapture event occurred on 2 May, 2008, and the fish was returned alive. The second recapture occurred on 12 November, 2008, but was kept by the fisher. During concurrent visual surveys of fish assemblages on these study platforms (Martin and Lowe 2010), eight resightings of tagged individuals occurred (four sheephead, two grass rockfish, and two kelp Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 665
Figure 2. Daily detection plots of tagged (A) cabezon, Scorpaenichthys marmoratus, (B) grass rockfish, Sebastes rastrelliger, (C) kelp rockfish, Sebastes atrovirens, and (D) sheephead, Semicossyphus pulcher. Each vertical dash indicates the presence of individuals on a given date at platform Edith (gray dashes), Elly (blue dashes), and Eureka (black dashes). Tag IDs are grouped by platform and sorted in descending order by the number of days that individuals were detected over the course of the study. rockfish); all appeared to display normal behavior and were sighted on their platform of original capture. Site Fidelity Long-term site fidelity analysis found 80% of sheephead, 61.5% of grass rockfish, 58.3% of kelp rockfish, and 50% of cabezon individuals were present at platforms at the end of the study after being at liberty for up to 578 d (Fig. 2). A higher percentage of cabezon displayed long-term site fidelity to platform Eureka (71.4%) than platform Edith (28.6%; chi-square: χ2 = 18.05, df = 1, P < 0.001). Comparisons of long-term site fidelity between platforms were not significantly different for grass rockfish (Edith: 57.2%, Eureka: 66.7%; χ2 = 0.728, df = 1, P = 0.34), kelp rockfish (50%, 66.7%)(χ2 = 2.39, df = 1, P= 0.12), and sheephead (87.5%, 71.4%; χ2 = 1.63, df = 1, P = 0.20). Fifty-five of the 63 fish tagged were detected a mean of 66.9% (SD 36.0%) of their total days at liberty (397–578 d), while being detected a mean of 372.8 (SD 201.2) d (Table 2). Individuals at platforms Edith and Eureka were detected a mean of 73.6% (SD 32.1%) [423.7 (SD 166.8) d] and 59.5% (SD 39.1%) [320.0 (SD 222.5) d] of their total days at liberty, respectively (Table 2). Twelve fish were detected 100% of their days at liberty, including three grass rockfish (560, 563, and 579 d), three kelp rock- fish (570, 571, and 572 d), and six sheephead (446, 543, 564, 571, 575, and 577 d; Fig. 2). Comparisons of daily site fidelity between platforms Edith and Eureka were not 666 Bulletin of Marine Science. Vol 95, No 4. 2019
Table 2. Summary of the minimum, maximum, and mean (SD) percentage of days that each species was detected at platform Edith, Eureka, and both platforms combined (Total) during their times at liberty from 17 June, 2008, to 15 January, 2009.
Number Min percentage Max percentage Species/ of fish of days detected of days detected Mean percentage of Mean number of Platform analyzed (number of days) (number of days) days detected (SD) days detected (SD) Cabezon Edith 8 2 (11) 94 (512) 69.0 (29.0) 371.4 (163.1) Eureka 7 3 (18) 98 (557) 53.3 (38.5) 299.3 (216.4) Total 15 2 (11) 98 (557) 61.7 (33.5) 337.7 (186.4) Grass rockfish Edith 7 33 (184) 100 (565) 70.1 (31.5) 391.4 (173.9) Eureka 6 24 (130) 100 (572) 52.6 (37.0) 299.3 (211.9) Total 13 24 (130) 100 (572) 62.0 (33.8) 348.9 (190.0) Kelp rockfish Edith 5 24 (139) 100 (573) 80.4 (32.7) 460.6 (187.3) Eureka 7 1 (3) 100 (572) 33.0 (44.4) 188.6 (254.5) Total 12 1 (3) 100 (573) 63.1 (42.4) 301.9 (260.2) Sheephead Edith 8 16 (91) 100 (573) 86.0 (28.8) 481.0 (160.8) Eureka 7 50 (288) 100 (578) 89.8 (19.1) 490.0 (103.2) Total 15 16 (91) 100 (578) 87.8 (24.0) 485.3 (132.3) All species Edith 28 2 (11) 100 (573) 76.2 (29.4) 423.7 (166.8) Eureka 27 3 (18) 100 (578) 57.4 (39.9) 320.0 (222.5) Total 55 2 (11) 100 (578) 66.9 (36.0) 372.8 (201.2) significantly different for cabezon (Mann-Whitney U = 68.00, df = 14, P = 0.684), grass rockfish U( = 55.5, df = 12, P = 0.39), kelp rockfish U( = 44.00, df = 11, P = 0.07), or sheephead (U = 57.5, df = 14, P = 0.487). At platform Edith, the mean daily site fidelity was 69.0% (SD 29.0%) for cabezon, 70.1% (SD 31.5%) for grass rockfish, 80.4% (SD 32.7%) for kelp rockfish, and 86.0% (SD 28.8%) for sheephead (Table 2). At plaform Eureka, the mean daily site fidelity was 53.3% (SD 38.5%) for cabezon, 52.6% (SD 37.0%) for grass rockfish, 45.8% (SD 47.3%) for kelp rockfish, and 89.7% (SD 19.1%) for sheephead (Table 2). Only one fish, a cabezon (ID# 2979) was detected at another platform other than its site of capture, which was found to move from plat- form Eureka on 7 July, 2007, to platform Elly on 17 July, 2007, where it remained until at least 15 January, 2009 (Fig. 2A). Comparisons of seasonal daily site fidelity for cabezon indicated they were de- tected a significantly lower proportion of days during summer than in fall (Mann- Whitney U = 46.50, df = 13, P = 0.016) and winter (U = 48.00, df = 13, P = 0.019; Fig. 3A). Grass rockfish were detected a significantly lower proportion of days during winter than fall (U = 43.00, df = 12, P = 0.019; Fig. 3B). No differences in seasonal daily site fidelity were observed for kelp rockfish (Fig. 3C) or sheephead (Fig. 3D). Depth Distribution, Habitat Use, and Temperature Effects Over the course of the study, all four species displayed some form of vertical move- ment (Fig. 4). Cabezon progressively used deeper areas of each platform during sum- mer, with detections ceasing completely by early September for two individuals at platform Edith (Fig. 4A). Cabezon displayed significant seasonal differences in depth Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 667
Figure 3. Seasonal daily site fidelity comparisons for (A) cabezon,Scorpaenichthys marmoratus, (B) grass rockfish, Sebastes rastrelliger, (C) kelp rockfish, Sebastes atrovirens, and (D) sheep- head, Semicossyphus pulcher among fall 2007, winter 2008, spring 2008, and summer 2008. Black horizontal lines within each box represent the species median daily site fidelity for that season and open circles represent the mean daily site fidelity. Seasonal categories that are sig- nificantly different P( < 0.05) from each other do not share the same letters, with “a” indicating the highest mean. Boxes represent the interquartile range (middle 50%) of data points, with the lower and upper line of the box extending to the 25th and 75th percentile of the data, respectively. The lower and upper whiskers extend to the minimum and maximum data points within 1.5 box heights from the box, with observations outside of these minimum and maximum values indi- cated by solid black circles. distribution (Kruskall Wallis: H = 159.45, df = 3, P < 0.001; Fig. 5A). They were de- tected at significantly shallower depths in winter when compared to fall, spring, and summer, and significantly deeper in summer when compared to all other seasons (Dunn’s post hoc test: P < 0.05; Online Appendix 1A). At platform Edith, 69.0% of all cabezon depth detections occurred within 3 m of horizontal levels, with 63.5% occurring within 3 m of the second horizontal level (30 m depth; Fig. 6). At platform Eureka, cabezon did not utilize horizontal levels as frequently, with only 17.6% of detections occurring within 3 m of horizontal levels (Fig. 6). Grass rockfish were primarily restricted to a shallow depth range (approximately 16 m) at both platforms Eureka and Edith; however, some individuals occasionally made short duration movements to deeper depths (approximately 30 m; Fig. 4B). Grass rockfish exhibited a significant change in seasonal depth distribution with individuals detected significantly shallower in spring (Fig. 5B) when compared to fall and winter (H = 83.20, df = 3, P < 0.001; Dunn’s post hoc test: P < 0.05; Online Appendix 1B). A majority of grass rockfish detections occurred within close proxim- ity of all horizontal levels on both platforms Edith (90.3%) and Eureka (99.4%), with most detections occurring within 3 m of the shallowest horizontal level on both plat- forms Edith (89.9%) and Eureka (99.4%) (Fig. 6). Kelp rockfish at platform Eureka were detected from shallow depths (approxi- mately 10 m) down to approximately 225 m, while individuals at platform Edith only 668 Bulletin of Marine Science. Vol 95, No 4. 2019
Figure 4. Time series depth plots (black line) of (A) cabezon, Scorpaenichthys marmoratus, (B) grass rockfish, Sebastes rastrelliger, (C) kelp rockfish, Sebastes atrovirens, and (D) sheephead, Semicossyphus pulcher individuals at platform Edith and Eureka overlying water temperature (°C) profiles (color gradient) measured from 5 to 30 m depths. Temperature is coded by color with red indicating warmer water and purple indicating colder water. Horizontal black lines at 50 and 212 m represent the bottom depth of platform Edith and Eureka, respectively. The first panel of Figure 4A displays the depth distributions of two different individuals, with tag ID# 198 displayed within the inset (box) and tag ID# 1 displayed normally. exhibited shallow depth use (15–30 m) over the duration of the study (Fig. 4C). A kelp rockfish (ID# 180) at platform Edith displayed its deepest depth detection (45 m) pri- or to loss of detections after 14 September, 2008 (Fig. 4C). Seasonal changes in kelp rockfish distribution were found H( = 99.47, df = 3, P < 0.001; Fig. 5C), with individu- als displaying significantly shallower depth distributions in spring (approximately Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 669
Figure 5. Seasonal comparisons of mean daily depths for (A) cabezon, Scorpaenichthys marmoratus, (B) grass rockfish, Sebastes rastrelliger, (C) kelp rockfish, Sebastes atrovirens, and (D) sheephead, Semicossyphus pulcher. Seasonal groups that are significantly different P( < 0.05) from each other do not share the same letters, with “a” indicating the highest mean. Boxes represent the interquartile range (middle 50%) of data points, with the lower and upper line of the box extending to the 25th and 75th percentile of the data, respectively. The line within the box indicates the median and open circles represent the mean. The lower and upper whiskers extend to the minimum and maximum data points within 1.5 box heights from the interquartile range, with observations outside of these minimum and maximum values indicated by solid black circles. Note y-scale range differs for each species.
14.5 m depth) compared to all other seasons (Dunn’s post hoc test: P < 0.05; Online Appendix 1C). Most kelp rockfish depth detections occurred within 3 m of a hori- zontal level at platform Edith (91.8% of total detections) and Eureka (61.4%; Fig. 6). At platform Edith, 91.3% of detections occurred within 3 m of the shallowest horizontal level, while at platform Eureka, 41.5% of detections occurred within 3 m of the shal- lowest level and 18.4% of detections occurring shallower than the first level (0–13 m depths; Fig. 6). Sheephead at both platforms Edith and Eureka occupied depths between 10 and 55 m, with individuals primarily detected between 10 and 20 m (Fig. 4D). One female sheephead (ID# 195) displayed an opposite behavior by primarily being detected deep (50 m) and making occasional movements to shallow depths between June 2007 and December 2007, after which it used shallow areas until detections ceased in mid- September 2008. Distinct patterns in movement to deeper depths were displayed by some sheephead during late summer, fall, and winter periods (Fig. 4D). These move- ments resulted in significant differences in sheephead seasonal daily depth useH ( = 135.16, df = 3, P < 0.001; Dunn’s post hoc test: P < 0.05; Online Appendix 1D), which consisted of a significantly deeper depth distribution in winter (approximately 30 m) and shallower distribution in spring and summer (approximately 15 m; Fig. 5D). At both platforms, 58.1% of all sheephead depth detections occurred within 3 m of 670 Bulletin of Marine Science. Vol 95, No 4. 2019
Figure 6. Percentage of species-specific depth detections associated with specific horizontal lev- els (shaded gray bars) and depths in between horizontal levels (nonshaded areas) at platform (A) Eureka and (B) Edith. Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 671 a horizontal level (Fig. 6). At platform Edith, 42.1% of the total depth detections oc- curred within 3 m of the first horizontal level with 38% of the total depth detections occurring shallower than the first level (0–11 m depths; Fig. 6). At platform Eureka, 57.0% of all depth detections for sheephead occurred within 3 m of the first horizon- tal level, with 27.6% of the total detections occurring shallower than the level (0–13 m depths; Fig. 6). During the study period, the warmest water was recorded between June and October in both 2007 and 2008, and the coldest temperatures occurring from March to mid-April 2008 at depths as shallow as 10 m (Fig. 4). There was a pronounced ther- mocline from June to December 2007, and May to December 2008 with a uniformly cold (13–14 °C) water column from mid-December to March 2008 (Fig. 4). The daily mean temperature difference between 5 and 30 m depths was found to have a sig- nificant effect on the daytime depth distribution of sheepheadH ( = 33.419, df = 6, P < 0.001; Fig. 7A) and the daily depth distribution of cabezon at platform Edith (H = 129.76, df = 7, P < 0.050; Fig. 7B). Results from Dunn’s post hoc comparisons of depth distributions by temperature difference are reported in Online Appendix 2. Sheephead were detected significantly deeper (approximately 22–25 m) during times when the thermocline was nonexistent or minimal (<2 °C; Fig. 7A, Online Appendix 2A). Cabezon on platform Edith were detected significantly shallower during periods when the temperature difference ranged from 0 to 1 °C (approximately 27–29 m) and significantly deeper when the temperature difference increased beyond 6 °C (Fig. 7B, Online Appendix 2B).
Discussion
Platform Site Fidelity Daily and long-term site fidelity metrics were utilized in the present study to char- acterize the importance of platform habitats to the four study species. Daily site fi- delity is used to assess the daily presence of individuals at platforms, which can be used to indicate whether platform habitats support the daily biological requirement of individuals over time. Long-term site fidelity solely measures whether individuals were present at the end of the study and provides an estimate of the duration of time that individuals continue to use or revisit platform habitat, similar to how traditional mark and recapture investigations estimate site fidelity based on an initial capture and recapture event. On petroleum platforms in the SBC, Lowe et al. (2009) defined degrees of daily site fidelity as low (0%–30%), moderate (31%–60%), and high (61%–90%) based on the mean proportion of the days that individuals were detected out of their total days at liberty. Based on these criteria, all four study species would be considered to display high daily site fidelity to platform habitats when individuals from platform Edith and Eureka are combined (Table 2). When using these same criteria to compare between platforms, cabezon, grass rockfish, and kelp rockfish exhibit high daily site fidelity to platform Edith (50 m bottom depth) and only moderate daily site fidelity to the deeper platform Eureka (212 m bottom depth), with sheephead displaying high daily site fidelity to both platforms (Table 2). Considering these criteria, the high daily site fidelity of cabezon, grass rockfish, and kelp rockfish to platform Edith vs their moderate daily site fidelity to platform Eureka, may be related to our ability to detect 672 Bulletin of Marine Science. Vol 95, No 4. 2019
Figure 7. (A) Sheephead, Semicossyphus pulcher, mean daytime (09:00–16:59 hrs) depths (m) at both platforms Edith and Eureka and (B) cabezon, Scorpaenichthys marmoratus, mean daily depth (m) at platform Edith vs daily temperature (°C) differences between 5 and 30 m depths. Temperature difference categories that are significantly different P( < 0.05) from each other do not share the same letters, with “a” indicating the highest mean. Boxes represent the interquar- tile range (middle 50%) of data points, with the lower and upper line of the box extending to the 25th and 75th percentile of the data, respectively. The line within the box indicates the median and open circles represent the mean. The lower and upper whiskers extend to the minimum and maximum data points within 1.5 box heights from the interquartile range, with observations outside of these minimum and maximum values indicated by solid black circles. individuals during their times of residency and the proximity of platforms to nearby reefs. Detection efficiency tests on platform Edith found 67% of all transmitter signals between 15 and 30 m depths to be detected by receivers located at 15 and 25 m depths, which also suggests that 33% of signals are not detected. These findings dem- onstrate strong acoustic coverage at these depths, but it is not clear how detection efficiency changes as fish move deeper than 30 m. Range test results found platform receivers to have a mean detection range of 81 m, suggesting that receivers located Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 673 at 25 m depth had the ability to detect individuals down to at least 106 m depth, but it was likely that detection efficiency decreases as individuals move deeper. Mooring line receivers likely played a greater role in detecting individuals as they move deeper (>100 m), since our range tests found these receivers to have a mean detection range of 498 m, but only a detection efficiency of 19.4%. Considering that Claisse et al. (2015) reported the footprint of platform Eureka (5390 m2) to be considerably larger than the footprint of platform Edith (2590 m2), it is likely that the individuals had a greater chance of being detected on a daily basis at platform Edith during their times of residency. An extra receiver was placed within platform Eureka to increase moni- toring coverage; however, detection efficiency tests were not performed at platform Eureka to truly characterize detection performance at this platform. Findings that cabezon displayed significantly lower long-term site fidelity to plat- form Edith than to platform Eureka may also be due to the proximity of platform Edith to natural reefs of comparable depth. Platform Edith is approximately 1 km to the east of 150 Kelp Reef, which occurs in the same depth range (50 m) as platform Edith. In addition, Horsehoe Reef is located approximately 12 km to the northwest of platform Edith and occurs in depth ranges (20–30 m) similar to those depths used by individuals in this study. Southeast Bank is the closest (approximately 2 km distance) natural reef to platform Eureka; however, it is located in approximately 90 m depth, which is much deeper than the depths most commonly used by species in the pres- ent study. Considering the close proximity and similar depths of 150 Kelp Reef and Horsehoe Reef to platform Edith, individuals tagged at platform Edith may have been more likely to utilize nearby natural reefs vs tagged individuals at platform Eureka that do not have similar shallow natural reef options in close proximity. Sheephead displayed high daily site fidelity to both platforms; this species is rarely observed below 85 m (Love 1996), as was confirmed by depth-sensing tags, and is unlikely to emigrate from rock reef habitat (Topping et al. 2006, Logan and Lowe 2018). Overall, the observed levels of daily and long-term site fidelity are comparable with observations of other reef-associated species from both petroleum platforms and natural reef habitat (Starr et al. 2002, Lowe et al. 2003, 2009, Topping et al. 2006, Mireles et al. 2012, Logan and Lowe 2018). Findings that 50% of cabezon, 61.5% of grass rockfish, 58.3% of kelp rockfish, and 80% of sheephead were present at platforms at the end of the study (long-term site fidelity) are similar to previous studies that report cabezon, kelp rockfish, and sheep- head to exhibit high site fidelity to natural rocky reefs (Hartmann 1987, Topping et al. 2006, Freiwald 2009, 2012, Lindholm et al. 2010, Mireles et al. 2012). The con- tinuous and year-round presence of the majority of tagged individuals indicates the ability of SPS petroleum platforms to provide suitable habitat, food, and the potential of spawning resources to support critical life stages of these species. This conclusion is supported by observations of high densities of juvenile and young-of-year (YOY) rockfish (Martin and Lowe 2010), as well as both garibaldi, Hypsypops rubicundus (Girard, 1854), and cabezon guarding egg masses (CJB Martin, C Mireles, California State University Long Beach, pers obs). The year-round presence of adult cabezon, grass rockfish, kelp rockfish, and sheephead, particularly during their spawning pe- riods (Warner 1975, Love 1996, Adreani et al. 2004), suggests that these species are spawning at these platforms; however this cannot be confirmed from the present study. 674 Bulletin of Marine Science. Vol 95, No 4. 2019
Because of their high vertical relief and isolated nature, SPS petroleum platforms provide settlement habitat for large numbers of reef fish recruits, as well as transient pelagic species (Martin and Lowe 2010, Love et al. 2012). This provides a substantial increase in the density of prey during the spring and summer, and provides ample foraging opportunities, creating a highly productive habitat for piscivorous species such as rockfish and cabezon (Claisse et al. 2014). The high site fidelity of these near- shore reef fishes, combined with the negligible fishing pressure and high prey avail- ability, support previous conclusions that California offshore platforms may function as de facto marine reserves (Love et al. 2003), and that these platforms function like natural fish habitat. Other assessments of fish at petroleum platforms in southern California have shown a lower degree of site fidelity. In a study by Lowe et al. (2009), several species of deeper-water rockfish, as well as cabezon, were shown to have lower daily site fidelity to petroleum platforms in the SBC, due to a higher rate of movement away to natural reefs located around the Northern Channel Islands approximately 16 km away, as well as interplatform movements. However, compared to the SBC, shallow natural rocky reef habitat is limited on mainland locations on the predominantly sandy SPS (Pondella et al. 2005), with the nearest island habitat located at Santa Catalina Island approximately 29 km away. The lesser extent of natural reef habitat adjacent to SPS platforms compared to SBC platforms may have resulted in lower emigration rates in the present study due to reduced habitat options and associated risks with longer- range emigration. Because fish assemblages associated with western SBC platforms are dominated by rockfishes, many of which are known to exhibit ontogenetic shifts to deeper rock habitat as they mature, lower site fidelity of smaller individuals may be expected from shallower platforms (Lowe et al. 2009). However, SPS platforms are mostly dominated by warm temperate nearshore species, which are known to show relatively high site fidelity and are not known to make ontogenetic shifts to deeper habitats as they age (Topping et al. 2005, 2006, Lindholm et al. 2010, Mireles et al. 2012). Therefore, fish species found at the SPS platforms may be more dependent upon platform habitat to support them across age classes than deeper-water species that could utilize neighboring deeper rock reef habitats (>80 m; Lowe et al. 2009). Although nearshore reef fishes were observed to exhibit high site fidelity to the SPS platforms, there was limited evidence of movement among the adjacent platforms of differing depths. This is counter to observations by Lowe et al. (2009) and Anthony et al. (2013) at platforms in the SBC. In both these studies, individuals were noted to either move between neighboring platforms, or home back to platforms from which they were captured and translocated. The observed interplatform movements by Lowe et al. (2009) noted a shift of eight vermillion rockfish, S. miniatus, and one copper rockfish, Sebastes caurinus Richardson, 1844, from a shallow platform (63 m deep) to a moderately deeper platform (96 m). These movements were thought to be evidence of an ontogenetic shift, as individuals never returned to the platform from which they were originally caught and tagged. In the present study, only one individual, a cabezon, displayed interplatform move- ments. This fish, ID #2979, was tagged at platform Eureka on 18 June, 2007, where it was detected for 20 d. On 7 July, 2007, it emigrated from the deeper platform Eureka (212 m bottom depth) and was detected 10 d later approximately 2.3 km away at the shallower platform Elly (77 m bottom depth), where it remained for the duration of the study period. As cabezon are known to have high site fidelity and display homing Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 675 behavior when translocated over >14 km (Mireles et al. 2012), emigration from the deeper platform Eureka may have been due to pressures such as competition. Martin and Lowe (2010) found the densities of all platform-associated species, including grass rockfish, kelp rockfish, and sheephead, to be much lower at platform Elly than at platform Eureka, with only cabezon displaying a higher mean density at platform Elly [0.18 (SE 0.06) fish 100 −2m ] than at platform Eureka [0.07 (SE 0.02) fish 100 −2m ]. As the interplatform movement occurred during summer 2007, it is unlikely that it was made in response to elevated temperatures, as colder areas were likely available on the deeper platform (Eureka) from which it emigrated. In addition, it is unlikely that this movement was made for reproductive purposes as cabezon typically spawn in California from October through April (Love 1996). It is also possible that this movement was related to this individual homing back to platform Elly, because it remained at platform Elly until at least the end of the study. Depth Distribution During their residence times at both platforms, all species displayed some form of seasonal shift in their vertical movements and use of horizontal levels. Cabezon used the deepest regions of both platforms, but did show seasonal differences in depth use, preferring deeper depths during summer and early fall, and shallower depth habitat during their spawning period in late fall and winter. This pattern was likely influ- enced by water temperature. During late fall and winter, when there was a reduced or weak thermocline and colder water temperatures throughout the water column, cabezon utilized increasingly shallower (about 30 m) portions of the platform struc- ture compared to summer (about 55 m). Although the geographic range of cabezon extends from Sitka Alaska to Punta Abreojos in Baja Mexico (Love 1996, Eschmeyer and Herald 1999), cabezon are found typically in cool temperate waters north of Point Conception, where they inhabit shallow nearshore reef habitats (O’Connell 1953, Quast 1968, Lauth 1989). Because of this cooler habitat preference, it would be expected that cabezon would seek deeper, cooler water during summer and fall, re- quiring them to move to deeper regions, or leave the platform all together. Evidence of this was demonstrated during summer 2008, when two cabezon spent increas- ingly more time in close proximity to the bottom of platform Edith (40–50 m), before emigrating at the end of August. At the same time, at platform Eureka, one cabezon moved to utilize depths between 50 and 120 m, prior to returning to shallower water in fall. This deeper depth usage by cabezon during warm water periods is further supported by visual observations of cabezon at the bottom of platform Eureka made via submersible surveys in late September 2009 (MS Love, University of California, Santa Barbara, pers comm). This preference for cooler, deeper water may have also contributed to the lapses in detections (from increased acoustic shadows at deeper depths) resulting in lower daily site fidelity during summer. Grass rockfish were primarily observed in shallow water, approximately 16 m deep, at both platforms, but deeper forays did occur primarily during the winter, often to depths below 30 m. Although one of the shallowest-occurring rockfish species, with juveniles and adults favoring intertidal water with low relief structure (Love et al. 2002), they have been noted to move to deeper water in the winter, likely for spawn- ing activity (Limbaugh 1955, Buonaccorsi et al. 2004). Considering that grass rock- fish displayed significantly deeper depth utilization during winter 2008 (Fig. 5B), it is plausible that these movements were related to spawning activities. 676 Bulletin of Marine Science. Vol 95, No 4. 2019
Kelp rockfish used the entire vertical structure of both platforms during the study. The deeper depth use of individuals on platform Eureka (>220 m) was carefully ex- amined to determine whether these individuals were actually present at the plat- form when they were detected. Considering the absence of natural reef in detectable ranges surrounding platform Eureka, the accuracy of the tags (+10 m at depths >204 m), and reports of portions of this platform located in depths of 215 m depth (Claisse et al. 2015), it was decided that these individuals were likely present at the platform when detected. Kelp rockfish favored shallower depths during the spring, which could be in response to new foraging opportunities presented by the influx of YOY fish and pelagic species (Martin and Lowe 2010). Hallacher and Roberts (1985) found that YOY rockfish accounted for the highest percentage of kelp rockfish diets during upwelling periods. However, during the summer, when warmer water with a strong thermocline occurred at the platforms, kelp rockfish moved to deeper depths. Based on their average depth distribution, kelp rockfish appear to avoid water temperature >19 °C (Fig. 4C). Sheephead were mostly found in shallow water between 10 and 20 m deep, al- though they were shown to use depths as deep as 55 m at both platforms during the winter. The influence of temperature on sheephead behavior has also been demon- strated by Topping et al. (2006), who found sheephead individuals to expand their home ranges during winter and early spring. As sheephead at platforms can only expand their horizontal home ranges to the perimeter of the platform, the deeper use displayed at SPS platforms during winter may indicate daytime home range expan- sion to possibly forage on new or unexploited prey in deeper areas. Seasonal shifts in depth use by sex was observed for sheephead tracked at Anacapa Island (Lindholm et al. 2010), although sex related differences were not investigated in the present study. Habitat Preference Most of the fish species exhibited an affinity for the habitat provided by horizontal levels in the present study, likely using it in much the same way as seafloor habitat. This was most evident in grass rockfish, with 90.3% and 99.4% of depth detections occurring within 3 m of the shallowest horizontal level at platforms Edith (15 m) and Eureka (17 m), respectively. A similar observation was made by Carlisle et al. (1964), who noted grass rockfish at platform Hazel in the SBC to be mostly associated with the 12 m horizontal level. Given that grass rockfish are a predominantly shallow- water species with an affinity for low-relief structure, as well as their propensity to rest directly on the substratum, their high affinity for horizontal structure would be expected. Cabezon, another species with an affinity for cooler, shallow low-relief habitats that rests directly on the substratum, also displayed a high affinity for horizontal cross beams at platform Edith (69% of depth detections); however, this was predominantly at the second horizontal level (27–33 m). Interestingly, use of the horizontal levels at platform Eureka was limited to only 17.6% of the total depth detections. This may be due to the increased number of diagonal supporting cross beams of the jacket at the larger platform Eureka, where cabezon were visually observed using those structures between horizontal levels. Both kelp rockfish and sheephead displayed their highest percentage of depth detections in close proximity to the shallowest horizontal level on both platform Eureka and Edith. Surprisingly, with the exception of kelp rockfish on platform Edith, the second most important aspect of habitat used by both kelp Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 677 rockfish and sheephead consisted of the areas shallower than the first horizontal level on both platforms, which is supported by their behaviors of being more off the seafloor or as roving benthic foragers (Love 1996). This shallower habitat consists of many vertical pipes (termed conductors) and these two species appeared to use these habitats similar to how they use vertical strands of kelp in natural habitat. These findings of the importance of horizontal levels as habitat for the four study species are supported by other artificial reefs studies that have found reef fish to utilize mostly horizontal substrate when more vertically complex habitat is avail- able (Grove et al. 1989). The fish tracked in the present study appear to use the tops of these horizontal levels much like seafloor while using the undersides of the levels much like reef overhangs, crevices, or kelp canopy during sheltering and foraging activities. Considering these findings, any decommissioning option that eliminates shallow horizontal levels will likely remove important habitat for all four of the study species. The degree to which these species used the shallowest portions of these platforms is inconsistent with findings by Claisse et al. (2015), who concluded that partial re- moval of upper reaches of California offshore platforms would have minimal effects on standing stock productivity, with the one exception being platform Edith that was predicted to lose 79.9% of its total production. All other SPS platforms were estimated to lose minimal productivity due to the retention of deeper depths, which supports primarily cooler-water rockfish species as well as lingcod. Claisse et al. (2015) relied primarily upon submersible surveys that were conducted once annually between September and November. During this time of year, warmer water tem- peratures occur on the SPS along with a deeper thermocline (Fig. 4). Therefore, the impact of biomass loss from partial removal may be under-represented, not account- ing for seasonal differences in biomass (Martin and Lowe 2010) or changes in water temperatures that may restrict depth usage by nearshore reef species to the shallower regions. Furthermore, it may overlook the seasonal importance of shallow water re- gions for some species, namely the increased foraging opportunities presented in the spring and summer by recruitment of YOY fishes and schooling pelagics (Martin and Lowe 2010). Based on these observed behavioral responses to seasonally chang- ing conditions, it is likely that the partial removal option would have much greater impacts on these populations of economically-important, nearshore reef species as- sociated with platforms on the SPS. Management Implications Findings from the present study suggest that SPS platforms provide important habitat for adult nearshore reef fishes. The high degrees of both daily and long-term site fidelity exhibited by a majority of individuals indicate that individuals remain at SPS platforms for extended periods of time and that daily shelter and foraging needs are being met, while also supporting individuals of these species throughout their spawning periods. If spawning is indeed occurring among resident species at SPS platforms, their larvae have the potential to be transported to natural reefs in the Southern California Bight (Anthony et al. 2013). In addition, there was evidence that fish behave differently among platforms, but respond to changing environmen- tal conditions in much the same ways. The current reefing program adopted in California considers partial removal of the entire upper platform structure to a depth of 26 m (partial removal option), which is 678 Bulletin of Marine Science. Vol 95, No 4. 2019 designated at that depth to avoid obstructions to navigation. However, applying this removal strategy to the SPS platforms would eliminate the habitats favored by three of the four economically-valuable, nearshore reef species studied, as well as the por- tion of habitat utilized by all four species during their reproductive periods. Given the habitat selection documented here, retention of the structure to at least the first horizontal support level would be a better strategy for the enhancement of nearshore reef species. The decommissioning option of no removal would have the least effect on nearshore species currently residing at offshore SPS platforms; however, to date no platform off California has been fully retained, which is likely due to the high estimated costs of maintaining the structure (Claisse et al. 2015). Management decisions related to decommissioning options should consider the site fidelity and habitat use of platform fishes over extended periods to protect the most ecologically beneficial habitats. Although our study focused on shallow near- shore reef fish assemblages on SPS platforms, it is not known if deeper reef fish as- semblages observed on California platforms also use shallower regions of platforms on a seasonal basis. Fish species that prefer cooler water regions may not be present in shallow water portions of platforms at times when dive or submersible surveys are typically conducted. Without an understanding of seasonal changes in depth- specific habitat associations, the partial removal of any platform structure may alter or negate the resource benefits that reefing options are intended to provide to fish assemblages. The present study further supports the ecological value of SPS plat- forms as fish habitat and demonstrates the importance of understanding the role that the shallow regions of petroleum platforms play in supporting fish assemblages over time. This understanding is critical to accurately inform management decisions regarding the ecological costs and benefits associated with reefing options.
Acknowledgments
We thank B Wohlers, K Anthony, K Loke, C Mull, B Hight, S Trbovich, T Mason, E Jarvis- Mason, H Gliniak, G McMichael, J Ayres, B Rogers, A Bauer, K Jirik, T Farrugia, J Cvitanovich, L Zahn, H Zemel, and F Murgolo for their field assistance. We thank J Archie and A Monge for providing assistance with data management and analysis and M Mireles for reviewing this manuscript. We thank M Love for providing key insight into all aspects of this study and the anonymous reviewers who provided helpful comments and suggestions that greatly improved this manuscript. Thanks to the crew of platforms Elly, Ellen, Edith, and Eureka for their help and maintaining safety protocols during all diving operations. Funding for this project was provided by California State University Long Beach, USC Sea Grant, and California Artificial Reef Enhancement Program.
Literature Cited
Adreani MS, Erisman BE, Warner RR. 2004. Courtship and spawning behavior in the California sheephead, Semicossyphus pulcher (Pisces: Labridae). Environ Biol Fishes. 71(1):13–19. https://doi.org/10.1023/B:EBFI.0000043177.98895.f7 Anthony KM, Love MS, Lowe CG. 2013. Translocation, homing behavior and habitat use of groundfishes associated with oil platforms in the East Santa Barbara Channel, California. Bull South Calif Acad Sci. 111(2):1. http://dx.doi.org/10.3160/0038-3872-111.2.101 Bernstein BB. 2015. Evaluating alternatives for decommissioning California’s offshore oil and gas platforms. Integr Environ Assess Manag. 11(4):537–541. https://doi.org/10.1002/ ieam.1657 Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 679
Bohnsack JA, Sutherland DL. 1985. Artificial reef research: a review with recommendations for future priorities. Bull Mar Sci. 37(1):11–39. Bram JB, Page HM, Dugan JE. 2005. Spatial and temporal variability in early successional patterns of an invertebrate assemblage at an offshore oil platform. J Exp Mar Biol Ecol. 317(2):223–237. https://doi.org/10.1016/j.jembe.2004.12.003 Buonaccorsi V, Westerman M, Stannard J, Kimbrell C, Lynn E, Vetter R. 2004. Molecular ge- netic structure suggests limited larval dispersal in grass rockfish, Sebastes rastrelliger. Mar Biol. 145(4):779–788. http://dx.doi.org/10.1007/s00227-004-1362-2 Carlisle JG, Turner CH, Ebert EE. 1964. Artificial habitat in the marine environment. Resources Agency of California, Department of Fish and Game. Carr M, McGinnis M, Forrester G, Harding J, Raimondi P. 2003. Consequences of alternative decommissioning options to reef fish assemblages and implications for decommissioning policy. University of California. Marine Science Institute, Coastal Research Center, OCS Study/MMS 53. Caselle J, Love MS, Fusaro C, Schroeder D. 2002. Trash or habitat? Fish assemblages on off- shore oilfield seafloor debris in the Santa Barbara Channel, California. ICES J Mar Sci. 59 suppl:S258–S265. https://doi.org/10.1006/jmsc.2002.1264 Claisse JT, Pondella DJ II, Love M, Zahn LA, Williams CM, Bull AS. 2015. Impacts from partial removal of decommissioned oil and gas platforms on fish biomass and production on the remaining platform structure and surrounding shell mounds. PLoS One. 10(9):e0135812. https://doi.org/10.1371/journal.pone.0135812 Claisse JT, Pondella DJ II, Love M, Zahn LA, Williams CM, Williams JP, Bull AS. 2014. Oil plat- forms off California are among the most productive marine fish habitats globally. Proc Natl Acad Sci USA. 111(43):15462–15467. https://doi.org/10.1073/pnas.1411477111 Emery BM, Washburn L, Love MS, Nishimoto MM, Ohlmann JC. 2006. Do oil and gas plat- forms off California reduce recruitment of bocaccio (Sebastes paucispinis) to natural habitat? An analysis based on trajectories derived from high-frequency radar. Fish Bull. 104(3):391–400. Eschmeyer WN, Herald ES. 1999. A field guide to Pacific coast fishes: North America. Houghton Mifflin Harcourt. Freiwald J. 2009. Causes and consequences of the movement of temperate reef fishes. University of California, Santa Cruz. Freiwald J. 2012. Movement of adult temperate reef fishes off the west coast of North America. Can J Fish Aquat Sci. 69(8):1362–1374. https://doi.org/10.1139/f2012-068 Grove RS, Sonu CJ, Nakamura M. 1989. Recent Japanese trends in fishing reef design and plan- ning. Bull Mar Sci. 44(2):984–996. Hallacher LE, Roberts DA. 1985. Differential utilization of space and food by the inshore rock- fishes (Scorpaenidae: Sebastes) of Carmel Bay, California. Environ Biol Fishes. 12(2):91– 110. https://doi.org/10.1007/BF00002762 Hartmann A. 1987. Movement of scorpionfishes (Scorpaenidae, Sebastes and Scorpaena) in the Southern California Bight. Calif Fish Game. 73(2):68–79. Horn MH, Allen LG, Lea RN. 2006. Biogeography. In: Allen LG, Pondella DJ II, Horn MH, edi- tors. The ecology of marine fishes: California and adjacent waters. University of California Press: Berkeley, California. Lauth R. 1989. Seasonal spawning cycle, spawning frequency, and batch fecundity of the ca- bezon, Scorpaenichthys marmoratus, in Puget Sound, Washington. Fish Bull. 87:145–154. Limbaugh C. 1955. Fish life in the kelp beds and the effects of kelp harvesting. Scripps Institution of Oceanography. Lindholm J, Knight A, Domeier M. 2010. Gender mediated patterns in the movement of California sheephead in the Northern Channel Islands (eastern Pacific). Calif Fish Game. 96(1):53–68. 680 Bulletin of Marine Science. Vol 95, No 4. 2019
Logan R, Lowe CG. 2018. Residency and connectivity of three gamefishes between natural reefs and a large mitigation artificial reef. Mar Ecol Prog Ser. 593:111–126. https://doi. org/10.3354/meps12527 Love MS. 1996. Probably more than you want to know about the fishes of the Pacific Coast. Really Big Press, Santa Barbara, CA. Love MS, Caselle JE, Snook L. 1999. Fish assemblages on mussel mounds surrounding seven oil platforms in the Santa Barbara Channel and Santa Maria Basin. Bull Mar Sci. 65(2):497–513. Love MS, Caselle JE, Snook L. 2000. Fish assemblages around seven oil platforms in the Santa Barbara Channel area. Fish Bull. 98(1):96–117. Love MS, Nishimoto M, Clark S, Schroeder DM. 2012. Recruitment of young-of-the-year fish- es to natural and artificial offshore structure within central and southern California waters, 2008–2010. Bull Mar Sci. 88(4):863–882. https://doi.org/10.5343/bms.2011.1101 Love MS, Schroeder DM, Nishimoto M. 2003. The ecological role of oil and gas production platforms and natural outcrops on fishes in southern and central California: a synthesis of information. U.S. Geological Survey, Biological Resources Division. Love MS, Yoklavich M, Thorsteinson LK. 2002. The rockfishes of the northeast Pacific. Univ of California Press. Love MS, York A. 2005. A comparison of the fish assemblages associated with an oil/gas pipe- line and adjacent seafloor in the Santa Barbara Channel, Southern California Bight. Bull Mar Sci. 77:101–117. Love MS, York A. 2006. The relationships between fish assemblages and the amount of bottom horizontal beam exposed at California oil platforms: fish habitat preferences at man-made platforms and (by inference) at natural reefs. Fish Bull. 104(4):542–549. Lowe CG, Anthony KM, Jarvis ET, Bellquist LF, Love MS. 2009. Site fidelity and movement patterns of groundfish associated with offshore petroleum platforms in the Santa Barbara Channel. Mar Coast Fish. https://doi.org/10.1577/C08-047.1 Lowe CG, Topping DT, Cartamil DP, Papastamatiou YP. 2003. Movement patterns, home range, and habitat utilization of adult kelp bass Paralabrax clathratus in a temperate no- take marine reserve. Mar Ecol Prog Ser. 256:205–216. https://doi.org/10.3354/meps256205 Martin CJB, Allen BJ, Lowe CG. 2012. Environmental impact assessment: detecting chang- es in fish community structure in response to disturbance with an asymmetric multi- variate BACI sampling design. Bull South Calif Acad Sci. 111(2):119–131. https://doi. org/10.3160/0038-3872-111.2.119 Martin CJB, Lowe CG. 2010. Assemblage structure of fish at offshore petroleum platforms on the San Pedro Shelf of southern California. Mar Coast Fish. 2(1):180–194. https://doi. org/10.1577/C09-037.1 Mireles C, Nakamura R, Wendt DE. 2012. A collaborative approach to investigate site fidelity, home range, and homing behavior of cabezon (Scorpaenichthys marmoratus). Fish Res. 113(1):133–142. https://doi.org/10.1016/j.fishres.2011.10.008 O’Connell CP. 1953. Fish Bulletin No. 93. The life history of the cabezon Scorpaenichthys marmoratus (Ayres). Scripps Institution of Oceanography Library. Page HM, Culver CS, Dugan JE, Mardian B. 2008. Oceanographic gradients and patterns in invertebrate assemblages on offshore oil platforms. ICES J Mar Sci. 65(6):851–861. https:// doi.org/10.1093/icesjms/fsn060 Page HM, Dugan JE, Schroeder DM, Nishimoto MM, Love MS, Hoesterey JC. 2007. Trophic links and condition of a temperate reef fish: comparisons among offshore oil platform and natural reef habitats. Mar Ecol Prog Ser. 344:245–256. https://doi.org/10.3354/meps06929 Pietri D, McAfee S, Mace A, Knight E, Rogers L, Chornesky E. 2011. Using science to inform controversial issues: A case study from the California Ocean Science Trust. Coast Manage. 39(3):296–316. https://doi.org/10.1080/08920753.2011.566118 Pondella DJ II, Gintert BE, Cobb JR, Allen LG. 2005. Biogeography of the nearshore rocky- reef fishes at the southern and Baja California islands. J Biogeogr. 32:187–201. https://doi. org/10.1111/j.1365-2699.2004.01180.x Mireles et al.: Nearshore reef fish behavior on offshore petroleum platforms 681
Pondella DJ II, Zahn LA, Love MS, Siegel D, Bernstein BB. 2015. Modeling fish production for southern California’s petroleum platforms. Integr Environ Assess Manag. 2015/09/04 ed. p. 584–593. Quast JC. 1968. Observations on the food of the kelp-bed fishes. Calif Fish Game. 139:109–142. Schroeder DM, Love MS. 2004. Ecological and political issues surrounding decommissioning of offshore oil facilities in the Southern California Bight. Ocean Coast Manage. 47(1–2):21– 48. https://doi.org/10.1016/j.ocecoaman.2004.03.002 Sonu CJ, Grove RS. 1985. Typical Japanese reef modules. Bull Mar Sci. 37(1):348–355. Starr RM, Heine JN, Felton JM, Cailliet GM. 2002. Movements of bocaccio (Sebastes paucispinis) and greenspotted (S. chlorostictus) rockfishes in a Monterey submarine canyon: implications for the design of marine reserves. Fish Bull. 100(2):324–337. Topping DT, Lowe CG, Caselle JE. 2005. Home range and habitat utilization of adult California sheephead, Semicossyphus pulcher (Labridae), in a temperate no-take marine reserve. Mar Biol. 147(2):301–311. https://doi.org/10.1007/s00227-005-1573-1 Topping DT, Lowe CG, Caselle JE. 2006. Site fidelity and seasonal movement patterns of adult California sheephead Semicossyphus pulcher (Labridae): an acoustic monitoring study. Mar Ecol Prog Ser. 326:257–267. https://doi.org/10.3354/meps326257 Warner RR. 1975. The reproductive biology of the protogynous hermaphrodite Pimelometopon pulchrum (Pisces: Labridae). Fish Bull. 73(2):262–283. Westmeyer MP, Wilson CA III, Nieland DL. 2007. Fidelity of red snapper to petroleum plat- forms in the northern Gulf of Mexico. In: Patterson WF III, Cowan JH Jr, Fitzhugh GR, Nieland DL, editors. Red snapper ecology and fisheries in the U.S. Gulf of Mexico. Am Fish Soc Symp. 60:105−121. Wolfson A, Van Blaricom G, Davis N, Lewbel G. 1979. The marine life of an offshore oil plat- form. Mar Ecol Prog Ser. 1:81–89. https://doi.org/10.3354/meps001081
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