Columbia coast, while Feder & Keiser (1980) investigated ... crude oil (Feder et al., 1990) and marine terminal oper- ations on ..... We thank Ken Morgan of the.
THE VELXGER @ CMS. Inc.. 1997
(April 14,1997) The Veliger 40(2):121-130
ReproductiveTiming and Nutritional Storage Cyclesof Mytilus' trossulusGould, 1850, in Port Vald ez, Alaska, Site of a Marine Oil Terminal by ARNY BLANCHARD nNo HOWARD M. FEDER Institute of Marine Science,University of Alaska, P.O. Box 757220, Fairbanks, Alaska 99775-7220,USA
Abstract. MytiLus trossuluswas investigated to determine the reproductive and nutritive cell storage cycles for this mussel in Port Yaldez, a fjord within Prince William Sound, Alaska. Three intertidal sites within the boundaries of a marine terminal, and four sites remote from the terminal area were sampled. Mussels from Port Ya|dez exhibit a distinct annual cycle with gametogenic development throughout winter, during periods with freezing air and water temperatures,and demonstratea summerlong spawning period. Nutritive cellsgenerally decreasethroughout late winter as gametogenesisproceeds to spawning, reaching minimal values during early summer. No differences between sites attributable to the proximity of mussels to the terminal area were apparent. The effects of stress,likely related to silt-laden waters derived from a nearby glacier, were observed at one site remote from the marine terminal. Regional differences in the reproductive cycles of MytiLus spp. are discussed.
INTRODUCTION Most previous studiesof musselson the northern Pacific coast were presumed to investigate the life history of MytiLusedulisLinnaeus, 1758 (Seed & Suchanek,1992). Recent literature indicatesthat MytiLustrossulusGould, 1850, the speciespreviously thought to be M. edulis,ranges along the Pacific coast from California to the Shumagin Islands, -lhus, Alaska (McDonald et al., 19911' Geller et al., 1994). Emmett et al. (1987) documentedthe reproductive cycle for M. trossulus,rather than M. edulis, for the British Columbia coast,while Feder & Keiser (1980) investigated M. trossulus,rather than M. eduLis,in Alaskan waters. Stereological analysis of mantle tissue has been used extensively to document the reproductive and nutritive storagecycles for Mytilur spp.in laboratory and field studies (seereview in Seed & Suchanek, 1992). Four stagesof the reproductive cycle-developing, ripe, spawning, and spent-are identified as primary categoriesuseful in describingreproductivetiming and events(Seed& Suchanek, 1992). In mussels, nutrients are stored in the adipogranular cells (ADG) and vesicular connectivetissue (VCT), which are the primary reservesof energy for reproduction (Gabbott & Peek, 1991). The main factors controlling reproduction and nutritional storage cycles are thou65htto be temperature and food availability. However, these cycles are apparently flexible, as mussels are able to adapt
to individual environmentsquickly (..g., Lowe et al., 1,994). No studiesare available that integrate reproductive timing and nutrition storage cycles for Alaskan mussels. Port Valdez is the terminus for a pipeline transporting crude oil from Prudhoe Bay, Alaska. Prior to receiving their oil cargo, tankers offioad oil-contaminated ballast water at the marine terminal, which is processedonshore at a treatment plant and then discharged into the port (Colonell, 1980). A seriesof studies,initiated in the mid1970s, indicated no or minor influence of Prudhoe Bay crude oil (Feder et al., 1990) and marine terminal operations on intertidal flora and fauna within Port Valdez ( e . g . ,S h a w e t a l . , 1 9 8 6 ; F e d e r & B r y s o n - S c h w a f e l1, 9 8 8 ; Anthony, 1995).An oil spill in outer Prince William Sound in March 1989 demonstratedthat the potential for a major oil spill is always present wherever oil tankers operate. However, chronic exposure to hydrocarbons (e.g., small oil spills, naturally occurring seeps,and pollution from boat traffic) -ay be a greater concern for marine organisms (Kennish, 1992). Sublethal responsesby musselsto stress (e.g.,chronic exposureto hydrocarbons)include reductions of nutritive reservesand reproductivetissues;delayed,reduced, or suspendedspawning; and increasedgamete degeneration and resorption (Myint & Tyler, 1982; Arimoto & Feng, 1983; Lowe & Pipe, 1986; lVfcCormick-Ray, 1987; Lowe, 1988). This paper examinesthe reproductive and nutritive cell cycles of Alaskan intertidal populations
Page1,22
The Veliger, Vol. 40, No. 2
oI' M. trossuLus adjacent to and remote from the manne terminal in Port Yaldez and compares thesecyclesto those reported for MyttLus spp. elsewhere.
THE STUDY AREA Port Valdez (61oN, 146'30'W) is a fjord located within Prince William Sound, a subarctic embayment of the northeastern Gulf of Alaska. The shoreline consistsof steep,rocky shores in the western end rvhich merge into low-profile cobble beachesand extensivemud flats to the east. The mean annual air temperature is approximately 1OoC,with sub-freezingtemperaturesin winter of -4o to -10oC, and a recordlow of -34"C (Hood et al., 1973). Surface-water temperature ranges from - 2oC in winter to 16'C in summer (Jervett & Feder, 1977). The tidal range is approximately 6 m (Colonell, 1980). The port receives increased freshwater runoff and sediment loads from glacial rivers and streams from lvlay to October resulting in low salinity (approaching )Vcn)and a high sediment load in the upper water layer (10 m). No heavy sea ice forms in Port Valdez. Primary production in the port is typical of high latitude marine systemswith a spring bloom in March-April and decreasedproduction through the summer (Goering et al., 1,973).A minor bloom occurs when the water turns over in fall. In winter, production ceases.Initiation of spawning by musselsis coincidentwith the occurrence of the spring bloom. Adult mussels are abundant intertidally and rare subtidally. Juveniles settle subtidally on algae or directly within mussel beds (Feder & K e i s e r , 1 9 8 0 ; F e d e r & B r y s o n - S c h w a f e l ,1 9 8 8 ) . T h e dominant invertebrate predators on musselsare the gastropod Nucella (abundant only on western shores where they prey on musselsthroughout the year), and the seastars Euasteriastroschelli (Stimpson, 1862) and Pycnopodiahelianthoides(Brandt, 1835) (important predators on rocky shores and cobble beaches;Feder & Bryson-Schwafel, 1988). From spring to autumn, a freshwater lens prevents seastarsfrom reaching intertidal mussels,but in winter, following a fall turnover, surface salinity increases, and thesepredatorsforage within the intertidal zone. The sea otter feedson musselsthroughout the port all year (Anthony, 1995). Seabirdsoccasionallyprey on mussels(Hogan & Irons, 1988).
METHODS Three intertidal sites-Berth 4 (B4), Ivlineral Creek (MC), and Sawmill Spit (SS)-were sampled from 1980 to 1982 (Figure 1) and four sites-Berth 5 (85), Saw Island (SI), Gold Creek (GC), and Five Mile Beach (5M)-were sampled from 1989 to 1991. 84, adjacenr to the marine terminal, is a moderately sloping beach with larse rock outcrops in the lower intertidal; musselsoccur in looselydefined clumps on the outcroppings. MC and SS are lowprofile cobble beaches,and musselsare widely dispersed
throughout the shore.The B5 site (200-300 meters west of 84) and 5lv{ are composedof steep rock faces, and musselsoccur at both sites in a well-defined bed on the rock face. GC and SI consist of moderately sloping rock outcrops)and musselsoccur in extensive,dense beds. 85 and SI are also within the terminal boundaries.Mussels were collectedmonthly from April, 1980 through September. 1982: some months were missed due to inclement weather. The 1989-1991 study assessedmussels from lvlar,:h to October, the months with highest biological activity. Sampling at SI was not initiated until April 1990. Surface-water temperature, salinity, and turbidity were collectedin conjunction with mussel sampling. Environmental data from another site, Anderson Bay, is presented as a proxy for missing data values in 1989 and 1991. Environmental data for 1991 were obtained from the Solomon Gulch Fish Hatchery, Valdez. Stereological techniques described for M. edulis elsewhere are used here. Mussels of various sizes(between20 mm to the maximum size of 60 mm) were collected and fixed with I0To Baker's formal-calcium solution and stored in 7Ct%ethyl alcohol. Histological preparation of mantle tissuc followed proceduresoutlined by Lowe et al. (1982). Point counts of reproductive tissuesin stereologicalanalysis were summarized according to four categories-developing, ripe, spalvning, and spent-derived from Seed (t97ti) and Kautsky (1982) (see also Seed & Suchanek, 1992). Nutritive cells were categorizedfollowing Lowe et al. (1982) into the adipogranular (ADG cells: containing proteins and lipids) and vesicularconnectivetissue(VCT: containingmostly glycogen)categories(Lowe et al., 1982). Poinl counts were made with a Weibel type-Z grid at each of 42 endpointsper field of view for 15 slidesfrom separate mussels.Five fieldsof view were examined from one tissue section for each slide. Volume fractions were calculated accordingto Lowe et al. (1982) as the sum of point counts for a categorydivided by the total number of countspossible (210",. Statistical procedures were applied to assessdifferences betweenpopulations.Nonparametric two way rank ANOVA comparisons(the Friedman test), with time (date of collection) as the factor and population location as the treatrnent (Lowe et al., 1994), were used to compare mean point count data, and multiple comparisonswere applied when significant differences (a < 0.05) were observed. Comparisons included mean point counts for active reproductivetissue(the sum of developing,ripe, and spawning categories);the ADG and VCT categories;total nutritive tissue (the sum of ADG and VCT categories);and the ADG:VCT ratio (Lowe et al., \982). Months in which not all sites were sampled and periods where data were not sampled monthly were excluded. For the 1989-1991 study, a l:riori N{ann-Whitney rank sum tests were used to compare proportions of reproductive and nutritive cells betwr:ensites within the terminal area-B5 and Sl-and thoseoutside of the terminal area-5M and GC. Pearson correlation values (r' and r2) between reproductive and
A. Blanchard & H. M. Feder, 1997
Page1,23
Shoup Glacier
MineralCreek
Valdez Glacier
Valdez
obeRiver Five Mile Beach
Terminal A L A S KA
Porl Voldez
Figure 1 Map of intertidal sitessampledin 1980-1982 and 1989-1991. Sitessampled in 1980-1982 are Berth 4, Sawmill S p i t , a n d M i n e r a l C r e e k . S i t e s s a m p i e d i n 1 9 8 9 - 1 9 9 1 a r e B e r t h 5 , F i v e M i l e B e a c h ,G o l d C r e e k , a n d S a w I s l a n d .
nutritive storagetissue volume fractions were determined f o r t h e t i m e p e r i o d sN o v e m b e r 1 9 8 0 t o S e p t e m b e r1 9 8 1 , November 1981 to September,Ivlarch to October 1990, and March to July 1991. The coefilcientof correlation (r) determines the direction (increasing or decreasing)and strength of the relationship between variables.The coefficient of determination (r2) measuresthe amount of variation within each variable that is accountedfor by any relationship between the variables.Both are useful statistics that measurethe associationof variables,in this case, the reproductiveand nutritive storagecycles. RESULTS Observed surface-water temperature ranged from -2oC during winter to 14oCduring sunlmer (Figure 2). Surfacewater salinity ranged from )Vc': in summer to 33%cntn winter. Surface-waterturbidity ranged from 0.6 mg I I to 244.3 mg l-1 (the winter maximum) with a summer maximum of 209.6 mg I '. N'Ieansurface-waterturbidity tended to increaseduring summer, but winter valueswere often high as a result of storms and winter winds. The reproductiveand nutritive cyclesfor musselsin Port Valdez are shown in Figures 3 and 4. Volume fractions of developingfollicles were typically first observedin No-
vember and increasedthroughout the winter. Ripe follicles were typically observedin March-April and occasionally occurredas early as February. In March of 1991, unusually high proportions of ripe follicleswere observedat all sites. Spawning follicles were generally observedin low proportions by lv{arch-April and high proportions by May and June. The proportion of spawning folliclesgenerally decreasedafter July and were presentin low volume fractions through September-October.The proportion of adipogranular cells(ADG) gradually decreasedthrough winter and into early spring, the months of early- to midgametogenesis.Volume fractions of these nutritive cells generally reached low values (approaching a minimum volume fraction of zero) during lvIarch, April, and May ( e . g . ,B e r t h 4 ( 8 4 ) 1 9 8 1 , 1 9 8 2 ) p r i o r t o s p a w n i n g . T h e ADG cells generally increased in June to a maximum summer peak in July or August and were variable in fall and early winter with a secondpeak occasionallyobservable in September-Octoberto January. Vesicular connective tissue (VCT) volume fractions VCT also showed decreasesthrough the winter but remained relatively high compared to ADG cells. The VCT cells usually reached minimum values between Aprii and June and increased in the following months, with peaks often occurring in August and again in January. Minimum proportions of
The Veliger,Vol. 40, No. 2
Page124 16
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A. Blanchard& H. M. Feder.1997
Page1,25
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fractions of cell categories for the 1980-1982 study period. The vertical axes are Tovolume fraction for the
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VCT cellsgenerally occurredabout two months later than minimum values for ADG cells. DecreasedVCT cell volumes generally coincidedwith increasedvolume friictions of ripe and spawning follicles. Some statistical differences were observedin data from both study periods.Comparisonsbetweensitessampledin 1980-1982, using two way rank ANOVA with factor and
treatment as time and location, demonstrated significant differencesfor the gametic tissue (P < 0.001) and VCT tissuescategories(P : 0.005). The multiple comparisons demonstrated that 84 had significantly higher quantities of mean reproductivetissues(P < 0.05) and lower quantities of mean VCT tissuesthan the Mineral Creek (MC) and Sawmill Spit (SS) sites.SS demonstratedsignificantly
Page1,26
The Veliger, Vol. 40, No. 2
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Page1,27
A. Blanchard & H. M. Feder. 1,997 Table 1 Pearson product moment total nutritive
coefficients of correlation
Site Berth 4 Berth 4 Mineral Mineral Sawmill Sawmill
(r) and coefficients of determination
(r2) bet.veen total gametic and
tissue volume fractions. The negative r values signify that total nutritive cell volume fractions decrease as total gametic volume fractions increase. n : sample size.
Creek Creek Spit Spit
Berth 5 Berth 5 Five Mile Beach Five Mile Beach Gold Creek Gold Creek Saw Island Saw Island
Months
12
Nov. 80-Sep. 8 1 Nov. 81-Sep.82 Nov. 80-Sep. 8 1 Nov.81-Sep.82 Nov. 80-Sep. 8 1 Nov. 81-Sep.82 Mar. Mar. Mar. Mar. Mar. Mar. Apr. Mar.
9 0 - O c t . 90 91-Jun. 9 1 90-Oct. 90 91-Jun. 9 1 90-Oct. 9 0 91-.Jun. 9 1 9 0 - O c t . 90 91-Jun. 9 \
120 94 1,1,3 85 104 95
-0.842 -0.839 -o.699 -0.582 - 0.836 -0.816
0.709 0.704 0.489 0.339 0.699 0.666
