BULLETIN OF MARINE SCIENCE, 74(1): 129–141, 2004
EGG MASSES OF LOLIGO OPALESCENS (CEPHALOPODA: MYOPSIDA) IN MONTEREY BAY, CALIFORNIA FOLLOWING THE EL NIÑO EVENT OF 1997–1998
Louis D. Zeidberg, William Hamner, Keith Moorehead and Emery Kristof
ABSTRACT The commercial fishery for Loligo opalescens (Berry 1911) off the coast of California collapsed in 1998 following the 1997 El Niño event. Nonetheless, small schools of adult squid in non-commercial quantities routinely were attracted to night-lights below boats anchored near Monterey Harbor. Accordingly, Monterey Bay was searched for egg beds with sonar, an ROV, and with SCUBA during September and October 1998 to see if adults were spawning. Scattered egg masses were found with brown capsules in the cen- ter surrounded by more recently deposited white capsules with embryonic developmen- tal differences of at least eight days. Brown capsules may provide visual stimulus for repeated site-specific spawning, ‘hotspot’ lek behavior. The egg masses were composed of multiple cohorts with capsule dimensions highly correlated to developmental stage. Means of 164 (SD = 20, n = 193) eggs/capsule and 259 (SD = 212, n = 13) capsules/mass were found, with 152 egg masses in the most concentrated 1000 m2 of the egg bed. The expected number of eggs was 6.46 ¥ 106 for this 1000 m2. The sea star Asterina miniata (Brandt, 1835) was observed feeding on the egg masses 26 times in Monterey Bay. In the laboratory the A. miniata and the gastropods Kelletia kelletii (Forbes, 1850) and Cypraea spadicea (Swainson, 1836) ate Loligo eggs.
The California market squid, Loligo opalescens, fishery collapsed in 1998. Landings totaled 2894.3 mt (no landings from Monterey Bay), compared to record landings of 80,561.3 mt in 1996. By the summer of 1998, California squid fishermen were seeking federal disaster assistance. Some feared that the population would take years to recover. Since the fishermen were unable to find adults in Monterey during this time, we attempted to find evidence of the population from the early life stages. Despite the lack of harvestable adults, we found many egg masses present on the sea floor at the traditional fishing sites. The California market squid has been harvested in Monterey Bay, California since 1860 (Vojkovich, 1998). Furthermore, as groundfish landings have experienced declines, cephalopod landings have maintained or increased their levels due to release from com- petition and increased harvest by fishermen (Caddy and Rodhouse, 1998). Squid land- ings increased dramatically up to 1997, along with fishing effort, although for the past twenty years catches have dipped following El Niño events (Vojkovich, 1998). Unlike in Japan, South America, and South Africa where fishermen use lights and automated jigs to capture squid in non-mating schools, in California, reproducing adults are harvested ex- clusively in the spawning grounds using purse seines and light boats. The ecology of squid reproduction of other species of loliginids has been studied, and each species has subtle differences. In each species studied, females are stimulated to deposit their capsules in the immediate vicinity of other eggs, but the substrate in which this occurs varies. Loligo gahi (Orbigny 1835) attach their egg capsules 0.5–2.5 m off the substrate exclusively to the frondless kelp stipes of Macrocystis pyrifera and Lessonia sp. (Arkhipkin et al. 2000). Loligo pealei (Lesueur 1821) anchor eggs onto seaweed, pilings,
Bulletin of Marine Science 129 © 2004 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 130 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 1, 2004 or rocky substrates (Summers, 1983). Egg strands of Loligo vulgaris reynaudii (Orbigny 1841) are either attached to sand grains or low profile rocky reefs (Sauer et al., 1993). Eggs of L. vulgaris are deposited at 20–25 m depth on fixed or floating supports often near other eggs (Worms, 1983). The behavior of egg laying in this species has been de- scribed as a lek-based mating system wherein groups of males serve as a visual stimulus to attract groups of females to reproduce (Sauer et al., 1997). Peak landings of L. opalescens occur in the winter and spring in southern California and the summer and fall in Monterey Bay (Fields, 1965). Fields (1965) first described the life history of this species from sub-samples of adults from the fishery. Recksiek and Frey (1978) revisited issues of diet, predation, morphology, and ecology. Spawning adults have been reared from eggs in the laboratory (Yang et al., 1986). The egg beds that result from mass spawning events have been characterized in San Diego (McGowan, 1954; Okutani and McGowan, 1969), Monterey (Fields 1965), and Puget Sound (Shimek et al., 1984) using SCUBA diving, trawling, and laboratory experiments. Although egg cap- sules potentially provide a large amount of nutrition, previous research found no evi- dence of in situ predation on this unprotected food resource (McGowen, 1954; Fields 1965, Shimek et al., 1984), and MacGinitie and MacGinitie (1949) only briefly men- tioned an observation of the sea star Asterina miniatus (Brandt 1835) requiring 72 hrs to feed on egg capsules in the laboratory. Landings of California market squid have historically been smaller by an order of mag- nitude following El Niño years. Since 1981, annual landings following El Niño events average 4600 mt while the landings for non-El Niño years average 50,100 mt (
METHODS
FIELD SURVEY AND COLLECTION.—Cruises were conducted in Carmel Bay and Monterey Bays from September 14–October 9, 1998 aboard the R/V SEAWORLD UCLA. We used a Benthos Mini- ROVer MKII, a Remotely Operated Vehicle (ROV), fitted with a drive video camera (Sony HAD) with a 2.7 f1.1 lens, a zoom video camera (Sony xc-999) w/6–18 f2.8 lens, and a still 35 mm camera Benthos 3782 with a 15 mm f2.8 lens. A 30 cm ruler was mounted within the frame of view of both cameras to give scale to the images immediately in front of the ROV. A Trak Point tracking system on the ROV along with a differential GPS aboard the ship were used to map the area sur- veyed. ZEIDBERG ET AL.: EGG MASSES OF LOLIGO DURING EL NIÑO EVENT 131
To get a broad-scale measure of egg distribution in the Monterey and Carmel Bays, we con- ducted extensive surveys via ‘live boating’ (deployment of the ROV while underway) along the 30 m isobath. In Monterey Bay this isobath was surveyed from Del Monte Beach near Seaside to Point Piños. After the live boating surveys of the area, surveys of specific locations from Hopkins Marine Station to the breakwater of Monterey Harbor were conducted with the ship double anchored (bow and stern) to keep the wind from rotating the boat. Carmel Bay was surveyed via live boating on September 28, 1998. Areas in front of Pebble Beach golf course (Stillwater Cove), Carmel River Beach, Monastery Beach, and Point Lobos State Preserve were surveyed with double anchoring primarily along the 30 m isobath. No egg capsules were observed in Carmel Bay. Once the boat was anchored, the area underneath was initially scanned to the limits of the cable (100 m). If egg capsules were observed, complete coverage of the area was achieved with transects underneath the ship. Each transect covered 120 m2 (60 ¥ 2 m -camera view). Eight transects would provided complete coverage under the ship, so that an area of 60 ¥ 16 m (960 m2) was surveyed at each egg site. Of the 60 hrs of ROV survey time, nine hrs of video were recorded on Super VHS tape and analyzed for egg mass density and ecological and behavioral observations of animals in the vicinity of the egg masses. All animals observed in the videos were identified to species using guides in Miller and Lea (1972) and Morris et al. (1980). After determining the location of the egg bed with the ROV, SCUBA dives were made to collect squid egg capsule masses in large plastic bags. On September 21, five masses were collected. On September 28 and October 8 the capsules of four egg masses were collected. 2454 egg capsules from these 13 masses were maintained in running seawater and were counted and measured for length within three days of collection. EGG CAPSULE MEASUREMENTS.—Twenty-four egg capsules were sub-sampled from one egg mass of the September 21 collection, and 24 from each of the four masses collected during the Septem- ber 28 and October 8 dives. To avoid over-sampling large capsules, the capsules were selected for length (eight long, eight medium, and eight short) and fixed in 10% formaldehyde and later pre- served in 70% ethanol. Three of the capsule masses were too large to collect from the sea floor in their entirety, and these were sub-sampled at depth. The remaining capsules were returned to the egg beds. Thus, nine masses were measured for capsule length, width, chorion diameter, egg num- ber (excluding hatched or empty chorions), and developmental stage of embryo. Each capsule has a base with a short, flexible stalk that permits the capsule to gently rock back and forth in the ocean surge. Because the attachment strings were often stretched during separation of capsules, length measurements are reported herein from the tip of the capsule to the most basal egg. Each mass was given a letter designation based on date of collection: group A (one mass collected on September 21); group B (four masses collected on September 28); and group C (four masses collected on October 8). Analysis of developmental stages was compared to the condition of the capsule sheath, provid- ing evidence of multiple cohorts within individual masses. Developmental stage of the preserved egg capsules was determined by combining descriptions of Fields (1965) and Segawa et al. (1988). While Fields’ (1965) account of developing embryos is of L. opalescens, he separated development into 16 stages based upon time, not the 30 developmental stages based on organogenesis as de- scribed by Arnold (1965) for L. pealei. We use Segawa’s (1988) account of development in Loligo forbesi (Steenstrup 1841) because the ontogeny of L. opalescens is more similar to L. forbesi than L. pealei (Arnold, 1965). The only major difference is that the funnel of L. opalescens closes in developmental stage 22 instead of stage 24 as in L. forbesi. When any egg in a given capsule reached stage 28, there also was evidence of hatching of some eggs in the same capsule. Egg number and capsule dimensions decrease in hatching capsules, and these were therefore removed from the data analysis. Of the 216 capsules measured, three had no eggs and 20 more had a developmental stage of greater than 28 (where hatching was underway), and consequently only 193 capsules were used for the final data analysis. LABORATORY OBSERVATIONS.—Three species of sea stars were observed to rest atop egg masses in Monterey Bay, Asterina miniata, Mediaster aequalis (Stimpson 1857) and Pycnopodia helianthoides 132 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 1, 2004
(Brandt 1835). While our pictures led us to believe that the sea stars were feeding on the eggs, we had no proof of digestion of egg capsules. To test if sea stars, or other potential egg predators, were actually digesting the developing squid embryos, we collected L. opalescens egg capsules, three bat stars, A. miniata, and three individuals of two species of carnivorous snails, K. kelletii and C. spadacea, from an egg bed on the south side of Santa Cruz Island on December 4, 1998. The eggs, bat stars, and snails were brought to a closed seawater system at UCLA and maintained in separate tanks for ten days at 18.5oC. On December 14, 1998 ten capsules were placed in each of the three, 15-gallon tanks with one sea star. The carnivorous snails and ten L. opalescens capsules were put in a fourth tank. The sea stars did not orient to the intact capsules, perhaps due to a lack of a strong chemical signature from the intact capsule sheaths and the turbulent flow in the tanks. A week later, bat stars that were not fed were placed onto the egg capsules to determine whether sea stars digest egg capsules. We did not attempt to simulate in situ feeding conditions.
RESULTS
FIELD SURVEY AND COLLECTION.—Egg masses occupied areas ranging from 10 ¥ 5 cm (a few capsules) to 150 ¥ 100 cm (about 1000 capsules). Except for one location in front of Hopkins Marine Station where we observed a small mass of seven capsules and two adjacent individual capsules, all egg beds occurred between 36o 37.0150¢N and 36o 36.774¢N and between 121o 53.076¢W and 121o 53.482¢W at a depth of approximately 30 m (Fig. 1). This elongated bed in which egg capsules were repeatedly found had an area of 33.56 ha. All eggs were deposited in sandy substrate adjacent to low profile rocks. Not all transects were recorded onto videotape, and egg mass density varied for the 47 transects analyzed. Sixteen transects contained egg masses with 1–26 masses per transect, whereas 66% of transects did not have eggs. For the 960 m2 area of greatest egg concen- tration, we found an average of 19 masses/transect (SD = 4.5, n = 8), with a total of 152 egg masses, for a mean density of 16 masses 10 m-2. From the SCUBA collected masses, the average number of capsules/mass was 259 (SD = 212, n = 13) and the average number of eggs/capsule was 164 (SD = 20, n = 193). 164 eggs/capsule ¥ 259 capsules/mass = 6 2 42,476 eggs/mass. For the 152 observed masses we estimate 6.46 ¥ 10 eggs in 960 m . Speckled sanddabs, Citharichthys stigmaeus (Jordan and Gilbert, 1882) were the most common vertebrates in the vicinity of the masses. The annelid worm Capitella ovincola (Hartman 1969) was commonly observed living within the gelatinous matrix of the egg capsules. The worms actively migrated out of brown capsules to infest neighboring white capsules in laboratory tanks. The sea star A. miniata was the most common invertebrate associated with squid egg beds either in the sand near or atop the capsules. For all transects analyzed, the number of sea stars within the camera view (2 m) of egg masses averaged 9.91 sea stars 120 m-2 transect (SD = 11.83, n = 47), or 0–3.83 A. miniata 10 m-2. We observed three species of sea stars resting on top of the egg capsules in the field on 30 occasions: Asterina miniata (26 times, 87% of feeding events), Mediaster aequalis (three times), Pycnopodia helianthoides (once). In each case the sea stars were resting atop the capsules with the central portion of their bodies bulging. We examined the sea stars directly via use of SCUBA. In each case when the sea stars were overturned their stomachs were everted. Citharichthys stigmaeus was observed on three occasions biting the capsules at scarred areas where the eggs were swelling out of the capsule sheath. Rhinogobiops nicholsii (Bean, 1882) [Blackeye goby] also bit at the areas of the capsules where the sheath was punctured. ZEIDBERG ET AL.: EGG MASSES OF LOLIGO DURING EL NIÑO EVENT 133
Figure 1. Map of the ROV survey area, Monterey Bay: Lovers Point to Monterey Harbor. ROV Surveys were conducted September–October 1998. Circles indicate the location of a transect survey. Filled circles indicate presence of egg capsules and clear circles indicate survey area with no egg capsules observed. HMS is Hopkins Marine Station. Inset: map of Monterey Bay, survey location in box. SC is Santa Cruz, California.
EGG CAPSULE MEASUREMENTS.—All capsules within each of the 13 masses collected were counted and measured for length (Table 1). Of the 2454 egg capsules measured, the average length was 84.7 mm (SD 22.8, range 15–152 mm). Length measurements of the egg masses from the three collections were normally distributed. There were no signifi- cant differences in length (ANOVA, P > 0.05 df = 12) among any of the masses except mass one and four of group B (ANOVA, P < 0.01, df = 12). These two samples were sub- samples of large masses, which may have affected the ANOVA. Of all parameters measured, length of capsule was most related to width of capsule (Correlation Z-test, r = 0.773). Capsule length and width were correlated with develop- mental stage, up to stage 28; developmental stage: width r = 0.582, and stage: length r = 0.573, (Table 2). From linear regression we found egg number = 1.867* capsule length, R2 = 0.898 (n = 192, P < 0.0001; Fig. 2). Based upon analysis of developmental stages and the condition of the capsule sheath, we found three distinct types of egg masses: 1) White masses contained small white capsules with thick and undamaged sheaths and embryos in the early stages of develop- ment; 2) Brown masses contained longer capsules that had wrinkled and cavitated sheaths with dark indentations, and perforated areas covered with sand and debris, and with de- 134 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 1, 2004
Table 1. Statistics of capsule lengths (mm): for masses collected in 1998 on September 21 (group A), September 28 (group B), and October 8 (group C).
Capsule lengths Mnass M.ea Sntd. dev Mxi Mna A61 735. 164. 32131 9 A22 932. 139. 30154 26 A63 710. 105. 29100 18 A74 685. 161. 259716 A25 713. 156. 16171 17 A2ll A 798. 158. 10124 88 B21 171 149. 32195 29 B12 750. 153. 23182 21 B73 696. 191. 269120 B74 961747103 22 A9ll B 81255. 22165 93 C31 932. 146. 32123 21 C92 991. 119. 40163 20 C93 557. 111. 389710 C14 908. 2635113 11 A4ll C 817. 212. 35163 63 A7ll Masses 884. 252. 12145 2,45
velopmentally advanced embryos; and 3) Mixed capsule masses had brown capsules in the center and white capsules around the periphery. The inner brown capsules were thin- ner and tore easily when measured. The eggs nearest the capsule perforations were often swollen with seawater. Of the nine masses sampled, five exhibited a mixed spawning history, with brown capsules surrounded by white capsules. On September 21, the range of developmental stages was 20–27, whereas on September 28 developmental range was 9–30, and on October 8 the range of stages was 12–30. Despite the range within each sample day, the mean developmental stage of white capsules was significantly different. (stage 19 SD = 4.8, n = 167), than the mean stage of the brown capsules, (stage 26 SD = 3.9, n = 45; Mann Whitney U-Test, P < 0.01; Fig. 3). Because brown capsules had more mature em- bryos than the white, the white capsules were most likely laid during a later spawning event. Stage 26 is eight days older than stage 19 when developing at 16oC. The develop- mental rate is even slower at colder temperatures and would be more than eight days apart at 12.8oC, the temperature at our field site for all collection dives in Monterey Bay at 30 m. Thus, peripherally located white capsules are the more recently laid, whereas the centrally located brown capsules were substantially older. Figure 3 shows frequency dis- tribution histograms of the developmental stages of white capsules compared to brown capsules, providing evidence of multiple cohorts within individual masses. LABORATORY OBSERVATIONS.—The sea stars, A. miniata, made no attempts to forage for the L. opalescens egg capsules in laboratory aquaria. However, once placed atop the capsules, the sea stars everted their stomachs over egg capsules and ate the squid em- bryos, with the sides of the digested capsules subsequently becoming dark, gray-brown. The agitation of capsules from the sea star feeding activity caused premature hatching of paralarvae. ZEIDBERG ET AL.: EGG MASSES OF LOLIGO DURING EL NIÑO EVENT 135
Figure 2. Linear regression of the number of eggs in a capsule regressed on egg capsule lengths. Number of eggs/capsule = 0 + 1.867 ¥ Capsule Length, r2 = 0.898 (P < 0.0001)
Within one hour of being placed into the tank with squid eggs, the predatory whelk, K. keletii, inserted its proboscis into four separate egg capsules, sweeping it back and forth, consuming the gelatinous matrix, the capsule sheath, and larval squid. After two days this snail had consumed large portions of four egg capsules and it had ceased feeding. The cowry, C. spadicea, also pierced the capsule sheaths and ate squid embryos. The feeding action of the snails stimulated hatching of neighboring embryos.
DISCUSSION
The egg masses of L. opalescens in the Monterey egg beds were white, brown, or mixed. The brown capsules that were comprised of older eggs, were infested with the annelid worm, Capitella ovincola, and had damaged sheaths. There are many potential causes of capsule damage, such as paralarvae hatching, worm infestation, predation from sea stars and/or sanddabs, and ocean surge repeatedly buffeting the capsules onto the surrounding sand. The in situ spawning behavior of L. opalescens has only been described from chance sightings with SCUBA (McGowan, 1954; Shimek, 1984). While we observed spawning adult squid only via sonar, never on film or on SCUBA, below we speculate about mating behavior based upon the details of our egg mass findings to enhance the planning of future behavioral experiments for loliginids. We believe the arrangement of older (brown) capsules surrounded by younger (white) capsules provides evidence for a ‘hot spot’ lek mating system. The presence of egg capsules rather than the presence of males stimulates spawning aggregations. Our observation that squid spawn repeatedly at the same site and immediately next to a prior set of egg capsules broadens the evidence for lek behavior in loliginids. Males may initiate lek-like aggregations in a general location, but the presence of first deposited capsules clearly fixes the location of successive spawnings. Squid for- age in small groups (100–200 individuals, Vaughn and Recksiek, 1979; Hunt et al., 2000), 136 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 1, 2004
Table 2. Number of capsules (n) and average of capsule dimensions measured for nine egg masses collected on September 21 (A1), 28 (B1-4), and October 8, 1998 (C1-4). Capsule dimensions include length (mm), capsule width (mm), diameter of eggs within the capsules (mm), mean number of eggs/capsule for each mass, and mean stage of developmental up to stage 28 when hatching begins for each mass.
Mnhass Lhengt Wmidt E#gg dia Eegg Stag A21 26936. 183. 43. 1731. 24. B41 281803. 194. 44. 1666. 22. B32 26753. 110. 33. 1140. 15. B43 29586. 98. 24. 196 14. B34 22970. 172. 38. 1486. 18. A4vg. B 91891. 161. 34. 1864. 17. C651 1504. 194. 45. 1391. 23. C32 28955. 123. 49. 1563. 23. C43 25539. 98. 24. 1175. 16. C44 2294153. 46. 1474. 22. A7vg. C 76823. 192. 38. 1870. 20. A3vg. all 149 82172. 34. 186 19.
and are stimulated to spawn by the presence of eggs (Fields, 1965; Hurley, 1977; Yang et al., 1986). Presumably visually stimulated by the eggs, the squid may remain in the area of egg masses. Group after group of adult squid may aggregate near the eggs into a spawn- ing mass. Males, therefore, probably do not exhibit ‘hotspot’ lek behavior, i.e., spawning aggregations assembled near particularly attractive males (Beehler and Foster, 1988), but instead the presence of eggs may indicate a particularly favorable place to spawn repeat- edly, a ‘hot spot’ lek (Gibson, 1996). Sauer et al. 1997 suggests for Loligo vulgaris reynaudii that “Males…assemble in large leks or lek-like aggregations to attract females and then compete for mating success. Daily offshore-to-inshore movements and circling aggregation of male squid draw in new male and female schools from offshore, increasing the size of the aggregation and the number of females.” But, they (Sauer et al. 1997; figure 1) show that all of their tagged females and sneaker males arrive on the egg beds at dawn, and while many of the large tagged males also arrive at dawn, their numbers do not peak until 1000 h. In re- peated laboratory observations, it is the presence of egg capsules, not males, that stimu- lates female L. opalescens squid to lay capsules (Fields, 1965; Hurley, 1977; Yang et al., 1986). This is true also for other species of loliginid squids (Summers, 1983; Worms 1983; Sauer et al., 1993; Arkhipkin et al., 2000). Predation may be an important source of mortality for squid eggs and hatchlings. Al- though Fields (1965) did not observe predation on squid eggs in situ, our observations show that there are at least some natural predators at spawning sites. We observed the bat star, A. miniata, feeding on eggs more frequently than any other predator, 26 out of 30 observations in the field, as confirmed by digestion of squid eggs in our laboratory study and by MacGinitie and MacGinitie (1949). The carnivorous gastropods, K. kelletii and C. spadicea, also vigorously ate eggs within capsules in the lab. Although these two species of snails are rare in Monterey Bay and rarely venture off rocky bottom habitats, these gastropods may be predators of importance on squid eggs in southern California, where 90% of the commercial population occurs. These snails found egg capsules in turbulent laboratory aquaria within one hour, but bat stars did not orient rapidly to the capsules and ZEIDBERG ET AL.: EGG MASSES OF LOLIGO DURING EL NIÑO EVENT 137
Figure 3. Histograms of the developmental stage of (A) white egg capsules and (B) brown egg capsules. Mean developmental stage (±SD) of white capsules, (19 ± 4.8, n = 167), was significantly different than the mean stage of the brown capsules, (26 ± 3.9, n = 45, Mann Whitney U-Test, P < 0.01). Scale for X and Y-axes are different.
took up to 48 hrs to begin feeding. The presence of these snails may explain why L. opalescens only lay their eggs in sand, providing a powerful, evolutionary forcing mecha- nism to enhance the survival of eggs not laid on rocks. Several species of fish were observed on the egg beds, including large numbers of the speckled sanddab, Citharichthys stimaeus, and blackeye gobies, Rhinogobiops nicholsii. Both of these species were observed biting at exposed eggs of brown capsules on mul- tiple occasions. Sanddabs also regularly swam amongst the egg capsules and carefully inspected particulate objects stirred up by the ROV by sucking the particulates into their mouths and spitting these out. Morejohn et al. (1978) examined the stomach contents of many local flatfish in Monterey Bay; Loligo opalescens was the most important food item for the Pacific sanddab, Citharychthys sordidus and for the curlfin turbot, Pleuronichthys decurrens. Some had eaten in excess of 600 post-hatch Loligo (2–3 mm 138 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 1, 2004
ML). Hatchling L. opalescens emerge at night (T. Preuss, Hopkins Marine Station, pers. comm.; Yang et al., 1986, Vidal et al., 2002). Clearly, hatchlings that remain near the bottom in daylight could draw the attention of visually hunting flatfish, providing a natu- ral selection for nighttime hatching. The annelid worm, Capitella ovincola, was often found within squid egg capsules (MacGinitie and MacGinitie, 1949), even those left in the natural environment for as little as one week (Fields, 1965). Abbott and Reish (1980) suggested that annelid worms initiate premature hatching. Worms migrated from brown infested capsules to white uninfested capsules in aquaria (LDZ, pers. obs.). Vidal et al. (2002) postulated that C. ovincola migrate from neighboring sand to the capsules and then eat the matrix jelly and possibly the microorganisms of the capsule sheath. Further we observed that worm infes- tations co-occur with a decrease in sheath thickness, exposure of eggs, and premature hatching. Even though there were no landings of adult squid in Monterey Bay in 1998, we ob- served egg beds in the region. Although the only actual spawning event we observed was on September 7, multiple cohorts must exist within one egg bed because of the presence of multiple developmental stages within a given spawning mass. Squid eggs develop faster in warmer water (Boyle et al., 1995; Villanueva, 2000; Forsythe et al., 2001). McGowan (1954) found that L. opalescens eggs took 35 d to hatch at 13.6oC, and Fields (1965) found that at 16oC, the difference between developmental stages 12 and 30 was more than three weeks. At 12.8oC in Monterey Bay, the time difference of capsule depo- sition within the masses collected on September 28 (developmental stages 12–30) must have been more than three weeks, with spawning events perhaps as long as a month apart. The disparate and asynchronous developmental masses that we observed provide clear evidence of multiple spawning events occurring throughout the month. Thus, although we only observed spawning once, and although there were no commercial landings that year in Monterey Bay, L. opalescens spawning occurred on a small scale, periodically and repeatedly, in September and October 1998. Our results show that squid do not always die after spawning, because the number of eggs far outnumbered the few dying adults on the spawning beds. During our 60 hrs of daily ROV observations we saw three individual adult squid among the capsules on three occasions, all spent, as evidenced by mantle atrophy and scarring. Egg beds of L. opalescens have been described as littered with the dead and dying bodies of adults (Fields, 1950, 1965; McGowan 1954; Hall and Hall, 1997). These observations obtained during limited SCUBA dives led many scientists in the past to conclude that L. opalescens and other loliginids are always semelparous. However, some loliginids spawn more than once. For example, Lipinski et al. (1998) and Sauer et al. (2000) found L. vulgaris reynaudii, spawning at separate locations five days apart and migration between spawning sites up to 207 km over 18 d. Maxwell and Hanlon (2000) observed multiple spawning events in L. pealei. Our observations of the presence of mixed-age eggs in the Monterey egg beds and the absence of spent adults in September and October of 1998, therefore, is consistent with non-terminal spawning in L. opalescens. Using a large-scale acoustic tracking array and coded tags small enough to be carried by squid (Welch et al., 2003), future investigators could determine where L. opalescens lies along a spectrum from pure iteroparity to pure semelparity. Alternatively, the absence of spent adults in Monterey Bay may be explained by emi- gration from the spawning grounds before death or California sea lion, Zalophus ZEIDBERG ET AL.: EGG MASSES OF LOLIGO DURING EL NIÑO EVENT 139
californianus, predation. Nonetheless, management strategies that assume that all squid die immediately after spawning will underestimate the damage caused by purse seining spawning adults if that population would have continued to spawn a few days hence. We estimate that we found 6.46 ¥ 106 eggs in the most concentrated 960 m2 area of the egg beds. Leos (1998) found an average weight of 42 g/pre-spawn adult squid. Yang et al. (1986) found 1% of the estimated egg number in their rearing experiment reached repro- ductive maturity. Granted, laboratory aquaria with ample daily feedings and a lack of predators would only provide a best-case scenario for in situ mortality. If 1% of the eggs that we found survived, the potential biomass of these squid would be 2713 kg. After our survey the first landing made in Monterey Bay, California occurred nine months later on July 7, 1999 when one boat captured 3320 kg. There were no further landings in Monterey Bay until September 1999. Butler et al. (1999) found this squid to range from 6–9 mo in age at spawning. If this landing was from the cohort we observed in the egg stages it would represent 1.2% of the estimated adult equivalent biomass from the most concen- trated area of the egg beds. Egg number per capsule could be a useful tool for an assessment of the size of adult recruitment for the following season. Our average of 164 eggs per capsule (SD 64, n = 193) falls within the range of Fields’ (1965) estimate of 100–300 and that of Shimek et al. (1984) of 149 (SD 35, n = 40). But our figures are lower than those of Okutani and McGowan (1969), who found an average of 212 eggs per capsule (n = 10). Routine ROV surveys of egg beds may eventually lead to population estimates based on egg numbers, as is currently done with other fishes that spawn pelagic eggs (Lo et al., 1995). The severe drop in commercial landings of the California market squid in 1998 has caused concern among the fishermen of California about the future of the L. opalescens fishery. Temporal closures of the fishery have been demonstrated to be modestly effec- tive in management of the fishery in Monterey Bay (Leos, 1998). We suggest that spatial closures might also be an effective management tool. Protecting a few spawning sites will guarantee at least some undisturbed reproduction. If L. opalescens individuals spawn more than once, adults that spawn in spatial preserves may still be fished at other spawn- ing localities.
ACKNOWLEDGEMENTS
This research was funded by California Department of Fish and Game award # FG7334MR. The National Geographic Society donated the use of the ROV and its staff. We thank P. Hamner, J. Schneider, D. Lauritzen, W. McCarthy, and D. Weyrauch for their extensive contributions to the fieldwork. We thank D. Zimmer, P. Fong, R. Ambrose and three anonymous reviewers for their editorial comments. We thank M. and P. Shedd for the gift of the R/V SEAWORLD to UCLA.
LITERATURE CITED
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DATE SUBMITTED: August 20, 2002. DATE ACCEPTED: October 29, 2003.
ADDRESSES: (W.M.H) Department of Organismic Biology, Ecology, and Evolution University of Cali- fornia, Los Angeles, Box 951606, Los Angeles, California 90095-1606. (K.M., E.K.) National Geo- graphic Society, Photographic Division, 1145 17th St. NW, Washington D. C. 20036-4688. CORRE- SPONDING AUTHOR: (L.D.Z.) Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd., Moss Landing, California 95039, E-mail: