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Spatial and temporal variability of spawning in the green sea urchin Strongylocentrotus droebachiensis along the coast of Maine.

ABSTRACT The timing and spatial variation in spawning in the green sea urchin Strongylocentrotus droebachiensis (Muller) was investigated at three moderately protected sites in each of three geographic regions along the coast of Maine before the commencement of significant commercial harvesting. Urchins were sampled monthly (1987 to 1988) from subtidal hard bottoms, and test diameter (TD), height, total wet weight, and gonad wet weight were measured. To interpret reproductive and spawning patterns additional data were taken on habitat type, water temperature, salinity, urchin density, and diets. Over a range of TD (34.1-89.4 mm), 1,594 urchins were sampled. Gonad index (GI) increased as an allometric function of TD, and for urchins from the northeast and southwest regions, GI was independent of TD for animals [greater than or equal to] 64 mm. In the central region, the size at independence was [greater than or equal to] 55 mm. Analysis of variance with a priori, planned contrasts was used to quantify temporal changes in GI and spawning at two spatial scales (within and between regions). This information serves as a preharvest baseline for green urchin dynamics, analysis of reproductive cycles and spawning, and for current and future ocean changes. Gonad index and spawning varied seasonally, spatially and interannually. Gonad index increased during fall and early winter, and peaked in midwinter before a major spawning event in April at seven of nine sites. Gonad index ranged from 10% to 20% from December to April. Spawning [measured as a steep decline in GI (48%-78%) between successive sampling dates) occurred between early April and mid-May, except at one site in the central (Lamoine: March to April) and one in the northeast (Jonesport: May to June) regions. Gonad index patterns during spawning corresponded inversely to increasing seawater temperatures in the range of 2.5-5[degrees]C. Salinity, urchin density, and test size did not explain a significant proportion of the variability in mean GI through time. Diets consisted primarily of diatoms and microalgae on ledge, sediment, and coralline barrens and showed no regional trends. Sex ratio explained a significant portion of the variability in mean GI at only one site. Seawater temperature, however, explained 55%-77% of the variability in mean GI through time. Predicting when spawning occurs in natural populations is central to the sea urchin fishery by refining estimates of what are termed harvest windows (HW). The HW represents a segment of time during the general spawning season when GI are at, or above, a specified percent, for example, 10%. A review of the literature uncovered 19 different techniques to determine GI and assess spawning. Of 167 papers published between 1922 and 2013 in which methods of spawning in wild populations of sea urchins were described, 84 and 134 used histology and GI. respectively. This study contributes to the questions of dependence of GI on test size, first illuminated by Gonor (1972), and the general practice of interpreting minor declines in GI as fractional spawning events, rather than simply sampling noise. The use of statistical tests is encouraged to define aspects of the reproductive cycle in sea urchins.

KEY WORDS: green sea urchin, Strongylocentrotus droebachiensis, Maine, gonad index, spawning, spatial and temporal variability, gonad-test diameter relationship, fractional spawning, harvest window

INTRODUCTION

Variation is a fundamental tenant of life in all its forms and expressions. Recognizing variability in individuals, populations, and communities allows ecologists to test hypotheses about processes affecting distribution, growth, and abundance patterns (Underwood et al. 2000). Growth, behavior, reproduction, recruitment, and other life history traits of marine populations are commonly varied over several spatial and temporal scales (Underwood & Keough 2001, Navarette et al. 2005, Lester et al. 2007). In some corals, for example, fecundity varies spatially between reefs because of differences in depth, turbidity, and sedimentation rates (Kojis & Quinn 1984). Temporal variability in algal-herbivore interactions occurs with Sargassum on reef flats in Australia (Leferve & Bellwood 2011). Similarly, year-class phenomenon related to poor reproductive success can affect recruitment strength in rockfishes (Sebastes spp.) (MacFarlane & Norton 1999).

Also, variability may result from the interaction of genetic and environmental processes (Trussell & Etter 2001). For example, early embryos of sea urchins (Centrostephanus rodgersii) experimentally stressed at gastrulation showed heritable variation in thermal tolerance suggesting the potential to adapt to ocean warming and acidification (Foo et al. 2012). Additionally, intraspecific variation in developmental mode (poecilogony) may be an adaptive response to unpredictable environmental conditions (Krug 2009) and variation in predatory behavior, reproductive strategy, and rates of early development is phenotypically plastic and has a genetic underpinning (Sanford & Worth 2009, Jackson et al. 2012). For example, the dispersal strategy of an estuarine polychaete (via planktotrophy or lecithotrophy) maintained population growth rates in less predictable or fluctuating environments (Levin et al. 1987). Conversely, synchronizing processes that increase opportunities for spawning and recruitment may mask and/or decrease variability (Lessios 1991).

Understanding the dynamics of commercial marine fisheries relies on quantitative observations that include the variability in spatial and temporal life history patterns. Stocks of ovigerous lobsters (Homarus americanus) displayed consistent spatial variation in density over several years at seven sites along a 190-km region of the Nova Scotia coast (Miller 1997). The collapse of northern cod (Gadus morhna) stocks of Newfoundland and Labrador was associated with spatial and temporal changes in density and biomass as well as high fishing mortality with declining stock biomass (Hutchings 1996). Also, variation in sea urchin life history traits can occur over short geographic distances (Byrne 1990). In Maine, for example, variation in longevity and test growth occurs in sympatric populations of green sea urchins Strongylocentrotus droebachiensis (Vadas et al. 2002) and differential growth and survival occurs across tidal gradients in populations of softshell clams Mya arenaria (Beal et al. 2001).

Variation in reproduction and spawning patterns in commercially harvested, temperate-boreal sea urchins also occurs both spatially and temporally (Byrne 1990, Byrne et al. 1998, Meidel & Scheibling 1998). Most cold water urchins undergo an annual reproductive cycle, but different populations of the same species may spawn asynchronously (Fuji 1960a, Himmelman 1978). Similarly, some tropical, subtropical, and deep-sea urchins show temporal and spatial fluctuations in their reproductive cycles (e.g., Moore & Lopez 1972, Tyler & Gage 1984, Muthiga & Jaccarini 2005).

Numerous mechanisms have been proposed to trigger reproduction (i.e., gametogenesis) and spawning in field populations of boreal urchins. Various environmental cues, such as temperature (Lamare & Stewart 1998, Agatsuma 2001a, 2001b), photoperiod (Walker & Lesser 1998, Dumont et al. 2006), lunar conditions (Lamare 1998, Byrne et al. 1998), and salinity (Starr et al. 1993, Vaschenko et al. 2001) have been implicated in stimulating spawning. Endogenous cues such as the release of pheromones have also been shown to cause spawning in green urchins (Pennington 1985). Also, biotic factors may play a direct or indirect role in spawning. For example, trophic subsidies, in the form of drift kelp, influence gonadal development and spawning in intertidal urchins (Tetrapygus niger) along the central coast of Chile (Rodriguez 2003), and subtidal urchins of the coast of Nova Scotia (Kelly et al. 2012). Lang and Mann (1976) demonstrated a significant density-dependent effect on gonad size in Strongylocentrotus droebachiensis in kelp beds versus coralline barrens. Increasing intraspecific densities and aggregative behaviors may result in mass spawning responses (Lamare & Stewart 1998, Gaudette et al. 2006) and Starr et al. (1990, 1992) demonstrated that elevated concentrations of phytoplankton (chlorophyll a) induced spawning in green sea urchins in the laboratory.

This study was conducted over a 270-km stretch (66%) of the Maine coast at three subtidal locations within each of three coastal regions (southwest, central, and northeast) in Maine, United States, between September 1987 and September 1988, before the development of a commercial fishery in Maine (Vadas et al. 2000, Fig. 1; Chen et al. 2003, Berkes et al. 2006) and recent concerns about effects of ocean and coastal acidification on reproductive success in sea urchins (Stumpp et al. 2012, Kurihara et al. 2013). The green sea urchin occurs along the entire Maine coast which covers several degrees of latitude and longitude. It is likely that over this distance, gradients in biotic and abiotic properties could contribute to substantial variation in growth and reproduction (see Morgan et al. 2000, Blicher et al. 2007).

These data and analyses provide a baseline for resource managers to evaluate and predict differences in reproduction brought about by harvesting strategies and possibly climate change. Also, they contribute to quantitative evaluations of size, spawning, and gonad index (GI) in sea urchin populations (Cocanour & Allen 1967, Vadas & Beal 1999). Reproductive patterns are linked to diet, life history, and environmental factors, and the results are discussed with respect to sea urchin management in Maine. In addition, a review of how spawning has been assessed historically in Strongylocentrotus droebachiensis and other regular echinoids provides an in-depth evaluation of the relationship between GI and TD. In this process it was discovered that 19 different measures of GI have been used (1922-2013) to assess spawning.

Recently, there has been a renewed interest in what induces spawning and the means of assessing it (Ebert et al. 2011, Ourens et al. 2012). Here, data are provided to assess spawning in Strongylocentrotus droebachiensis. Assumptions play a large part of deriving the formulae and logic in relying on the particular methodology used. This effort contributes to that dialog and to a new concept of "harvest windows" (HW).

STUDY SITES AND METHODS

General

In conjunction with the Maine Department of Marine Resources (DMR), nine sites were selected in a nonrandom fashion [i.e., based on ease of access for divers and from previous investigations (R. L. Vadas, unpublished data)] to reflect possible variation in reproduction and spawning in green sea urchins along the coast of Maine (Fig. 1, Table 1) (Vadas et al. 1997). Three general regions were specifically selected that ranged in linear distance from ~40 to 100 km, increasing in distance from the southwest to the central and northeast. Three moderately protected locations within each region were chosen based on urchin presence and diving accessibility from shore. Distance between research sites varied from a low of 7.7 km in the southwest to nearly 60 km in the northeast (Table 1). We consider these sites and regions as fixed factors in all statistical tests (see below). Urchins were sampled monthly from September 1987 to September 1988 by SCUBA from depths ranging from 2 to 8 m. To provide independence among urchins, 12-20 individuals [~40 mm (diameter) or larger] were sampled haphazardly each month along a belt transect. Animals were placed in coolers with seaweed and blue ice packs, returned to the laboratory, stored overnight at 4[degrees]C and dissected the following day. Sea urchin density and size were estimated at all locations, except Owl's Head, in May to June 1988 using 8-19 haphazardly placed quadrats (50 cm X 50 cm; Table 1). Temperature was measured monthly 15-30 cm beneath the surface using a calibrated stem thermometer. Salinity samples were taken at the same depth and analyzed using a hydrometer kit (G. M. Manufacturing Co.) and interpolated to the nearest part per thousand.

Site Descriptions and Habitat Quality

The three southwestern sites (Bailey Island, Five Islands, Boothbay Harbor) had similar, depauperate, floristic patterns. The understories contained relatively few macroalgae, were dominated by ledge with a high coverage of crustose coralline algae and bare rock, and were considered "barren grounds" (sensu Lawrence 1975). At Bailey Island, however, a few small scattered kelp plants formed a patchy structure. Two of the central coastal sites (Stonington and Lamoine) were categorized as barren grounds. These two sites contained no edible fleshy algae. Nonedible Desmarestia sp. and Agarum clathratum were present at both sites. Our characterization of the benthos at Owl's Head (Table 1) is based on monthly observations by divers. Moderately high urchin densities and high littorinid densities (200-300 per [m.sup.2], Vadas 1992) contributed to the impoverished macroalgal flora at Lamoine. Northeastern sites contained higher abundances of macroalgae, including edible kelp. In particular, the shallow sublittoral fringe at Schoodic Point had the highest proportion of kelp of the nine sites and had a moderate canopy of Saccharina latissima (formerly known as Laminaria saccharina) and Alaria esculenta. The deeper depths, however, were typical of barren areas and contained A. clathratum and coralline algal crusts. The sites at Jonesport and Lubec had a moderate fleshy algal cover, and in the understory, contained exposed ledge and coralline crusts. Several sites contained sparse, patchy kelp in the deeper depths, but most of this was A. clathratum, a nonpreferred kelp which often persists in the presence of urchins (Vadas 1977, Himmelman et al. 1983). Herbivorous gastropods, mainly Littorina littorea, were present at most sites, but during late spring were concentrated in the low intertidal and sublittoral fringe. Green urchins were the major macrograzers at most sites.

Gonad Index and Sex Ratio

Quantitative GI values were determined monthly from each site. Test diameter (range = 34.1-89.4 mm) using Vernier calipers were measured to the nearest 0.1 mm. This size range was based on Gonor's (1972) recognition with Strongylocentrotus purpuratus that GI may not be independent of body size below a 40 mm TD. Wet test weight was recorded to the nearest 0.1 g. The peristomial membrane and body cavity were then pierced, the coelomic fluid was drained, and the animals were weighed a second time. Sex was determined by observing sperm or eggs (when present) or making smears on microscope slides. Gonads were placed on paper towels, allowed to dry for 1-2 min, and then weighed to the nearest 0.1 g. Gonad index is a ratio expressed as gonad weight (or volume) divided by live test weight (or volume) X 100. The validity of using gonad weight as an alternative to gonad volume (GV) was tested over all populations for the initial two (September and October 1987) sampling intervals. Gonad volume (read as displaced seawater in a graduated cylinder) served as the dependent variable and was regressed against gonad weight [GV = 0.127 + (0.9323) X (gonad weight), [r.sup.2] = 0.994, n = 353]. In addition, analyses were conducted to test whether differences in the relationship between gonad weight and total (wet) weight occurred within and between regions.

Diet

To determine if GI was related to diet, quantitative estimates were made of prey items in the guts of urchins. The gut of five urchins (chosen randomly) was dissected and examined seasonally (late fall, late winter, spring, and summer = 34 sampling dates) from each site and placed in seawater with 10% buffered formalin to estimate temporal variation in diet. Two subsamples of fecal pellets were collected from each urchin and placed in separate beakers of seawater and stirred with a pipette to separate prey items. A 0.5-ml sample was pipetted onto a glass slide with cover slip. The area under each cover slip was examined and all algae and invertebrates were recorded and scored to obtain a relative estimate of frequency of occurrence. The relative importance of algal functional groups in the diet (Littler & Littler 1980, Steneck & Dethier 1994) was estimated from these counts. Data are expressed as relative abundance of each prey organism and as mean relative abundance of various algal functional groups (6 = abundant, 5 = common, 4 = present, 3 = infrequent, 2 = rare, 1 = absent). Thus, each site and date is represented by 10 counts from five urchins. Overall, a total of 180 urchins and 360 gut samples were examined.

Statistical Analyses

Comparison of GI, both temporally and spatially, assumes that GI is independent of urchin body size (diameter) (Gonor 1972, Ebert et al. 2011, Ourens et al. 2012). Because it was unfeasible to sort underwater all urchins at or above 40 mm TD on each sampling date, this assumption was tested using regression analysis with GI (dependent variable) and TD (independent variable). Generally, internal volumes and heights increase linearly with body size (Gonor 1972); therefore, analysis was begun by examining a linear model between these two variables. A sequential lack-of-fit analysis (Steele & Torrie 1980) was performed beginning with animals >45 mm TD. The lack-of-fit analysis used quadratic and cubic response variables. In addition, an allometric model was fit to the data.

To determine if GI varied temporally and spatially, a model I, two-factor analysis of variance (ANOVA) was performed using site and sampling date as fixed factors. The data were skewed and/or variances were heterogeneous before conducting an arcsine transformation (Sokal & Rohlf 1981). Because there was a highly significant interaction between site and date (P < 0.0001), using a model I, single-factor ANOVA, how GI varied temporally at each site was examined. The specific contrasts were based on observations before our study by Stephens (1972) who demonstrated that seawater temperatures near 4[degrees]C (both in the field and laboratory) were associated with green sea urchins from Maine and Massachusetts that were in a spawning condition. In addition, Stephens showed that the breeding season can be extended by 2 mo by holding ripe animals at 4[degrees]C. Also, field observations were made by Harvey (1956) and Cocanour & Allen (1967) who noted that temperatures above 4[degrees]C were associated with gamete release. For example, the first contrast ([[bar.x].sub.Jan.,Feb.,Mar.,Apr.] versus [[bar.x].sub.May,Jun.,Jul.]) was based on seawater temperature values <4[degrees]C versus [greater than or equal to] 4[degrees]C. The second contrast ([[bar.x].sub.Jan.,Feb.,Mar.] versus [[bar.x].sub.Apr.]) examined if GI changed significantly during winter. The third contrast ([[bar.x].sub.May] versus [[bar.x].sub.Jun.,Jul.]) tested whether changes in GI occurred when seawater temperatures were immediately >4[degrees]C. The fourth contrast ([[bar.x].sub.July] versus [[bar.x].sub.Aug.,Sept.]) tested whether a late summer/early fall (fractional) spawning occurs as in Newfoundland (Keats et al. 1987) and Nova Scotia (Meidel & Scheibling 1998). A conservative decision rule was used for the four contrasts ([alpha]' = 1 - [[alpha].sup.1/m]; where [alpha] = 0.05 and m = 4) based on Winer et al. 1991; therefore [alpha]' = 0.0127. Unplanned comparisons of mean GI between sampling dates were carried out using the Bonferroni corrected t-tests using a decision rule of [alpha] = 0.05, or the a posteriori StudentNeumann-Keuls (SNK) test. In addition, regional (fixed factor) and site-specific differences in mean maximum GI (reproductive potential sensu Lamare et al. 2002) were examined using a nested ANOVA followed by a posteriori SNK test.

Although the GI ratio was adjusted for differences in body size by attempting to sample urchins >40 mm TD, this may not have completely removed the effects of body size on this ratio (Packard & Boardman 1999, Harrington et al. 2007, Ebert et al. 2011). Therefore, the approach of Packard and Boardman (1999) and Ebert et al. (2011) was followed, and a more sensitive test [analysis of covariance (ANCOVA)] was conducted to determine the effect of date on reproductive cycle for each site. Least-squares regression lines were fitted to the data (gonad wet weight = dependent variable versus TD = independent variable). Slopes were compared using the least-square means for gonad wet weight to test for significant monthly variation in the dependent variable. In addition, a priori comparisons were used to test hypotheses concerning the least square means for pre-and postspawning events (as described above).

RESULTS

Sea Urchin Densities

Densities of sea urchins at the southwestern study sites were the highest of any region, but were highly variable, and ranged from 40 per [m.sup.2] to nearly 70 per [m.sup.2]. Individuals were aggregated at one of the three sites [Bailey Island; Morisita's Index ([I.sub.d] = 1.57, P = 0.002)]. Densities at central sites, Stonington and Lamoine, varied greatly (5 and 30 per [m.sup.2]. respectively), and were aggregated at Lamoine ([I.sub.d] = 1.16, P = 0.012). Among the northeastern sites, urchins at Schoodic Point were aggregated only at the deepest depth (6-8 m; [I.sub.d] = 1.48, P = 0.008) and were rare in the shallowest depth (Table 1), where moderate wave exposure and surge were common. Urchin densities differed dramatically between the two other northeastern sites. Only a single urchin was sampled in the 19 quadrats taken at the Jonesport site ([bar.x] = 1.3 per [m.sup.2]). The density estimate at this location may be biased low because of the shallow depth range of samples taken. Sea urchins were found mainly on boulders or ledge outcrops at Lubec where densities were moderately high (Table 1), and animals were not aggregated ([I.sub.d] = 1.87, P = 0.065).

Sea Urchin Sizes

Urchins collected at all sites averaged >60 mm TD (Fig. 2) and >30 mm in height (data not shown), except Lamoine where animals consistently had the smallest test sizes [[bar.x] [+ or -] 95% confidence interval (CI) = 49.7 [+ or -] 0.5 mm, n = 173]. Size-frequency distributions were not homogeneous among sites (G-test of independence, df = 24, P < 0.0001), and within each region (P < 0.0001). These data indicate that during the initial stages of intensive (4-fold increase) commercial harvesting, 1987 to 1988 (National Marine Fisheries Service 2014), the largest urchins occurred in the northeastern and southwestern regions of the state.

Validation of Gonad Index

Gonad index and urchin TD were related over the size range of animals sampled (Fig. 3). The allometric model (y = [ax.sup.b]) produced the highest coefficient of determination for these data (a = 0.004, b = 1.86, [r.sup.2] = 0.1437, n = 1594, P< 0.0001; Table 2). The relatively low coefficient of determination may be a related to the fact that these data (Fig. 3) include information from all sites and all sampling dates. Subsequently, the same relationship on a subset of the data was examined (for sampling dates with peak GI values for each site-March or April 1987). The relationship was similar to the complete data set ([r.sup.2] = 0.1393, n = 93, P = 0.0002). Therefore, the site-specific body size-GI relationship for the larger data set was examined and found that the slopes of the regression lines were significantly different (F= 9.43, df = 8,1576, P < 0.0001). For all data, a threshold TD was sought above which GI was independent of body size. Beginning at 40 mm, and testing in 5 mm increments, the four models presented in Table 2 were analyzed. At TD < 60 mm, each model yielded a statistically significant coefficient of determination. At TD [greater than or equal to] 60 mm, the linear, quadratic, and allometric models yielded highly significant P values, although [r.sup.2] values were low. At TD [greater than or equal to] 62.5 mm, only the quadratic model was statistically significant (Table 2). At TD [greater than or equal to] 64 mm, however, each model demonstrated that GI was independent of urchin size. This relationship was similar between urchin populations in the northeast and southwest regions, but differed in the central region where GI was independent of TD for animals [greater than or equal to] 55 mm.

Although GI depended on urchin size, and because our samples contained urchins as small as 34 mm TD, we decided to test if the pattern of GI varied differently through time for two size groups of urchins--all animals versus those [greater than or equal to] 64 mm TD. We used a conservative approach and selected one site within each region [Five Islands (southwest), Stonington (central), Schoodic Point (northeast)] where there was a prevalence of smaller sized individuals (Fig. 2). Analysis of variance was used to compare mean GI for the two size groups separately for each site, and demonstrated no significant sampling date X urchin group interaction (P> 0.55) or significant group effect (P > 0.15; Fig. 4). Because of the similarity of GI patterns between the complete versus reduced data set (i.e., the [greater than or equal to] 64 mm subset), we present mean GI data for the full range of urchin sizes from each site (Figs. 5-7).

Hydrography

Temperature patterns were similar throughout the three regions and followed a typical profile for cold subarctic-boreal waters. Several features are worth noting from these data (Figs. 5-7). Most sites, except Five Islands and Lubec, had temperatures at or below zero for one or more months. Summer temperatures were 2-10[degrees]C cooler (maximum 10[degrees]C) at eastern sites, which likely resulted from greater tidal amplitudes in eastern Maine along with increased mixing with bottom and Bay of Fundy waters (Garside & Garside 2004). The greatest range of temperatures occurred in the central region. Overall, temperature ranges were more similar at central and western sites.

Three general patterns are evident from the salinity data (Figs. 5-7). First, all sites were influenced to some extent by snow melt and runoff during late winter and early spring. Second, salinities at Bailey Island, Boothbay Harbor, Five Islands, Owl's Head, and Jonesport generally were in the higher range of values for the nearshore Gulf of Maine (29-34 psu except during April). Third, Stonington, Lamoine, and Schoodic Point consistently had the lowest salinities with Lamoine ranging into the low 20s.

Gonad Indices

Typically maximum GI occurred in late winter or early spring at the nine sites (Figs. 5-7). Significant temporal variation in mean GI was observed at all sites (P < 0.0001). Although there was a highly significant interaction between site and sampling date in the two-way ANOVA, some consistent patterns are evident in the reproductive cycle and spawning in sea urchins in Maine. In general, gonads enlarge during fall and early winter and urchins spawn in early spring. Gonad indices typically were lowest immediately after spawning and throughout summer. Indices began increasing during early fall. Mean GI for the nine sites ranged from a low of 2.4% (Lamoine, October 1987) to a high of 22.9% (Lubec, March 1988) (Figs. 5-7). Prespawning indices generally ranged from 14% to 19%, whereas postspawning indices ranged from 5% to 11% at all sites, except Lamoine and Stonington, which were lower. Gonad indices remained relatively low (x [+ or -] 95% CI = 8.3 [+ or -] 0.34, n = 600) from May through early fall during the recovery phase (sensu Fuji 1960b, Byrne 1990, Meidel & Scheibling 1998, Walker & Lesser 1998, Harrington et al. 2007). Generally, GI increased by 80% between November 1987 and February 1988, except at Lamoine where the increase was insignificant (ca. 2%).

We examined mean maximum GI loss between successive sampling dates, which we assume represents the major (i.e., annual) spawning period, for each site (Table 3). This loss in mean GI ranged from 48% to 78%, and generally occurred between April and May (Figs. 5-7). We analyzed these data by preplanned, orthogonal contrasts (Table 4; contrast 1), which demonstrated a significant decline (major spawning pulse) in mean GI between the January-April and May to July sampling dates at seven sites. This pattern did not occur at two sites [Lamoine, where spawning occurred between March and April (Fig. 6); Jonesport, where spawning occurred between May and June (Fig. 7)]. During the prespawning period (January to April) mean GI increased significantly at only three of the sites (Five Islands, Boothbay Harbor, Stonington) (Table 4; contrast 2). For example, the mean detectable increase in mean GI during this period was 7.4% whereas the mean increase at the other sites was <1 %. The same contrast for urchins at Lamoine was significant, but for a different reason. Mean GI increased from January 13 to March 16, 1988, but declined rapidly after this date (Fig. 6). No differences in mean GI occurred in larger urchins ([greater than or equal to] 64 mm) between January and April at any site (Table 4). Immediate (statistically significant) recovery of mean GI after spawning was detected at only two sites (Owl's Head, ca. 50%, Fig. 6; and Jonesport, ca. 60%, Fig. 7). No differences in mean GI were detected at any site from July to September 1988 for either the full data set or for the >64 mm set (Table 4; contrast 4); however, these tests may have been too conservative because August and September sampling dates were pooled, and Figure 5 suggests a fall spawning event at all sites in the southwestern region at the end of summer 1988, immediately after seawater temperatures had reached their annual maxima. The loss in mean GI also was associated with a 45.5%-76.7% loss in mean gonad wet weight over all sites ([bar.x] [+ or -] 95% CI = 61.1 [+ or -] 7.45%, n = 9).

Analysis of least-square regression lines (gonad wet weight versus TD) demonstrated homogeneous slopes for all months and sites (P > 0.15). For each site, analysis of adjusted gonad weights (least-square means) confirmed results (both overall F-test and preplanned contrasts) from the single-factor ANOVA on mean GI (Table 4). Mean GI, unadjusted, and adjusted mean gonad weight varied similarly through time at all sites, and an example from each region is presented (Fig. 8). These analyses indicate that the GI measurements (Figs. 5-7) are reasonable estimates of site-specific reproductive cycles (sensu Harrington et al. 2007), and highlight the utility (sensitivity) of this technique to discern patterns of reproduction (Packard & Boardman 1999, Ebert et al. 2011).

Further examination of mean GI versus mean temperature in the three regions (Fig. 9) indicates that GI decreases linearly with sea surface temperature for central and northeast urchin populations. The southwestern populations, however, appeared to respond differently as the addition of a quadratic term to the linear model was significant (P = 0.004), suggesting that mean GI increases with temperatures above 12[degrees]C. Seawater temperature explained 55%-77% of the variability in mean GI through time across the three regions (Fig. 9). A reanalysis of the August (mean GI = 12.2 [+ or -] 0.5%, n = 39) and September 1988 (10.1 [+ or -] 0.5%, n = 39) GI data for the southwestern populations (Fig. 5) was carried out to determine whether the apparent decrease [noise or possible fall (fractional spawning)] in mean GI (-17.2%) was statistically different from zero. We used the post hoc Tukey [honestly significant difference HSD)] procedure (Winer et al. 1991) which demonstrated that the two means were not equal (P < 0.01). A similar test for the central (n = 83) and northeastern (n = 84) populations for the same two sampling dates in 1988 showed that the mean difference in GI (+9.5%) was not significantly different from zero (P = 0.26). In addition, a fall spawning event may have occurred in 1987 at Schoodic Point (northeast; Fig. 7). One could ask whether the change in the transformed mean GI during the period between October and December could have occurred by random chance alone (F = 6.3; df = 2, 42; P = 0.0041). A Bonferonni test indicated that the 51 % decrease from October to November was statistically significant (P = 0.05). A similar analysis for Five Islands (southwest; Fig. 5; F = 2.68; df = 2, 42; P = 0.081) indicated no significant change in mean GI.

Mean maximum gonad index (max GI) varied between regions (Table 5). The Student-Neumann-Keuls test revealed that mean max GI did not differ significantly between the southwest and northeast regions (20.2 [+ or -] 1.5%, n = 79), and was ~52% higher than the mean maximum from the central region (13.3 [+ or -] 2.2%, n = 43). Only the central region showed significant site-to-site variability in mean max GI (Table 5). The Student-Neumann-Keuls test demonstrated that urchins from Owl's Head and Stonington had significantly higher max GI values (15.5 [+ or -] 2.3%, n = 28) than urchins from Lamoine (9.1 [+ or -] 4.1%, n = 15).

Inter- and Intraregional Differences in Gonad Weight versus Total Weight

The relationship between gonad weight and total weight of all urchins measured was weakly linear ([r.sup.2] = 0.442, P < 0.0001, n = 1586), but an allometric model gave a significantly better fit (a = 0.00347, b = 1.721, [r.sup.2] = 0.564, P < 0.0001). For the southwest and northeast regions, the log-transformed lines were not parallel (P = 0.011 and P < 0.001, respectively). The lines for each of the three sites within the central region were parallel (P = 0.1140), and an ANCOVA indicated that there was a significant difference between sites (P < 0.0001). Analysis of the adjusted means (sensu Packard & Boardman 1999) demonstrated that each site was significantly different from one another (P < 0.0001). Mean adjusted gonad weight (i.e., least-square means) for a given total weight for urchins at Owl's Head was 33.2% greater than urchins at Stonington, which was 94.7% greater than urchins at Lamoine.

Sex Ratio

Sex was determined in 977 (61.3%) of 1,594 individuals examined. The remainder (617 or 38.7%) could not be accurately sexed. Most of the ambiguity in gender occurred during the recovery phase (postspawning) between May and September 1988. Of the animals sexed successfully, the ratio was not significantly different from 1:1 (female = 505; male = 472; G = 1.115, df = 1, P = 0.2910). This ratio did not vary across regions (G = 5.128, df = 2, P = 0.0770), but differed significantly over sampling dates (G = 89.733, df = 13, P < 0.0001). For example, from June through September, the sex of 81 urchins (pooled over all sites) was determined and 69 (85%) were male (P < 0.025). In October. November, and February, females (n = 206) occurred in a higher proportion (62.8%) than males (n = 122; P < 0.05). In addition, sex ratio depended on sampling date at three of the nine sites [Boothbay Harbor: P = 0.0172, no bias (nb) =9, female bias (fb) = 3; Five Islands: P = 0.0313, nb = 6, fb = 2, male bias (mb) = 4; Schoodic Point: P = 0.0005, nb = 6. fb = 4, mb = 2].

Overall mean TD varied significantly as a function of urchin gender (P = 0.0006). Females were, on average, 1.7 mm larger than males ([[bar.x].sub.female] [+ or -] 95% CI = 64.6 [+ or -] 0.72 mm, n = 505; [[bar.x].sub.male] = 62.9 [+ or -] 0.70 mm, n = 472). In addition, mean GI pooled across all sites and sampling dates varied by sex (P = 0.0002). Females had a higher mean GI (13.2 [+ or -] 0.65%) than males (11.7 [+ or -] 0.47%). Overall mean GI of urchins that could not be accurately sexed (mostly during the post spawning period) was -30% lower than the average of those urchins whose sex was not ambiguous (8.5 [+ or -] 0.41%, n = 617).

Sea Urchin Diets

Twenty-eight taxa of algae were identified in the gut of green sea urchins from the nine sites and were categorized as five functional groups (Table 6). Gut analyses revealed that diatoms and microalgae were consistently the dominant prey items at our sites, accounting for nearly 80% of the algal items ingested. Diatoms were the dominant algal form in 19 of the 36 sample dates (based on site and season). The diet of urchins in the central and western region was dominated by diatoms. Microalgae (which included cyanobacteria, coccoid green algae, chrysophytes, individual cells and fragments, and relatively unbranched filaments of red, brown, and green algae) dominated 10 sample dates. Filamentous algae were the only other algal group of some importance in the guts of these urchins. Foliose forms and large macrophytes were unimportant components in the diet, and usually were rated as patchy and rare (2) or absent (1) (Table 6). In addition, six groups (mainly orders) of invertebrates were identified from gut analyses, but were rare or infrequent. These included amphipods, bivalves, cladocerans, isopods, nematodes, and ostracods. Although rare, these invertebrates occurred more often, in descending order, from Five Islands. Bailey Island, Owl's Head, Stonington, and Schoodic Point. Surprisingly, none were observed in individuals from samples taken at Lamoine, Jonesport, and Lubec.

DISCUSSION

Study Sites und Reproductive Patterns

In Maine, Strongylocentrotus droebachiensis has an annual reproductive cycle (Cocanour & Allen 1967, Vadas & Grant 1973, Vadas et al. 2000, Seward 2002, Gaudette et al. 2006, Harrington et al. 2007, this study). Urchins at the nine sites spawned between March and May. Similar annual cycles in wild populations of green sea urchins have been observed elsewhere in the northwest Atlantic Ocean (e.g., Himmelman 1978. Keats et al. 1984a, Meidel & Scheibling 1998). Relatively few studies on regular sea urchins have investigated reproductive cycles over the broad geographic scale encompassed by the three regions examined here (but see McPherson 1968. 1969. Pearse 1968, 1970, Byrne et al. 1998, Viktorovskaya & Matveev 2000, Kino & Agatsuma 2007, Lester et al. 2007). See also Ourens et al. 2011 for a geographic evaluation of reproduction in Paracentrotus lividus. In addition, Sivertsen and Hopkins (1995) found considerable variation in gonad growth and maturation of S. droebachiensis over a wide geographic scale along the Norwegian West Coast. A number of investigators have studied annual changes in gonadal weights or indices at single or multiple locations in close proximity (Bennett & Giese 1955, Lewis 1958, Himmelman 1978, Falk-Peterson & Lonning 1983, Munk 1992, Meidel & Scheibling 1998. Brady & Scheibling 2006).

Here, statistically significant changes in monthly GI were used to evaluate objectively when urchins spawned (Meidel & Scheibling 1998, Lamare et al. 2002), with the assumption that the maximum mean difference in GI between two successive monthly collections (range = 48%-78%; Table 3) represented the interval over which spawning occurred. Similar assumptions were made by Himmelman (1975) for Strongylocentrotus droebachiensis, and by Spirlet et al. (1998), Guettaf et al. (2000), and Leoni et al. (2003) for other urchin species. The analyses (Table 4) indicated a single, major spawning in late winter/early spring 1987 (Figs. 5-8). For example, spawning occurred between the April 6 16 and May 10-18 collections at seven of the nine sites. This was followed by a recovery period (summer) and a growth phase when gonad mass increased by nearly 80% (fall/early winter). This temporal pattern, however, varied within and between regions (Figs. 5-7). After November 1987 GI varied widely at the three southwestern sites, whereas spawning and recovery phases (April to September 1988) were relatively synchronous (Fig. 5).

Variation in reproductive patterns can occur over long (years) temporal scales at the same site. For example, in 2002, Gaudcttc et al. (2006) collected urchins near one of our southwestern sites near West Boothbay Harbor, ME, and showed that mean GI between March and May was greater (ca. GI 25%) than that was observed over a similar sampling date15 y earlier (ca. GI 15%). This difference could be explained by the return of kelp (Steneck ct al. 2002) (mainly Saccharina sp.) due to the reduced density of grazing sea urchins caused by commercial harvesting. Also, Gaudette et al. (2006) found that urchins spawned about 2-3 wk later than they did in 1987 (based on a biweekly mean that was 3.7 SD lower than the mean of their previous 10 sampling dates (Fig. 3 in Gaudette et al. 2006). In the central region, variation in the timing of spawning occurred between sites as urchins at Lamoine Beach spawned 1 mo earlier (March to April) than urchins at the other sites. In addition, mean GI at Lamoine was significantly lower (GI rarely exceeded 5%) than those at other central region sites in and on most sampling dates (Fig. 6). This is in contrast to what Cocanour and Allen (1967) found at the same site during 1965 to 1966, as mean GI was [greater than or equal to] 8% in 8 of 13 monthly samples. In the northeast region, gonad development in the fall/early winter of 1987 was more variable than the other two regions (Fig. 7). In addition, spawning in the northeast region was asynchronous as urchins at Jonesport spawned approximately 1 mo later (May to June) than those at the other two sites. Seward (2002) found that spawning in 2000 at the same Jonesport site (Table 1) occurred between early March and late May 2000. Taken together, these data indicate that spawning varies spatially and temporally along the Maine coast.

Assumptions about GI

Because GI is a relative measure of reproductive effort, it is not clear whether changes in this variable represent a real change in gonad mass or in one or more of the other variables. For example, in this study mean GI values on the sampling date before spawning (usually the peak value, Figs. 5-7) varied across the three regions from 12.9% to 19.5% and then declined to a mean ranging from 4.2% to 8.5% a month later (ca. 55%-65% decrease in 1 mo). It is important to note that the apparent loss of gonadal tissue may have occurred as a result of changes in spatial and temporal dynamics of coelomic fluid, food intake, and defecation, as implied by Fuji (1967). That is, gonad weight could remain constant through time, yet GI show peaks and troughs due to changes in gut fullness, fluid content, and/or diet, and this could affect the gonadal/somatic ratio (Leoni et al. 2003). Several studies have shown a strong, positive correlation between GI and availability of food (Fuji 1960a, Ebert 1968, Gonor 1973a, Spirlet et al. 1998) or food quality (Keats et al. 1983). Specifically, if diet and gut fullness were responsible for the observed changes in GI between pre- and postspawning dates (Figs. 5-7), then there should be no relationship between GI and gonad mass. Conversely, if a relationship exists between these two variables, the highest values of GI should be associated with the highest values of gonad weight before spawning. Concomitantly, the lowest GI values should be associated with the lowest values of gonad weight after spawning. Therefore, a positive relationship should exist between GI and gonad weight over these two sampling dates. Figure 10 shows a positive relationship between these two variables for each of the three regions, suggesting that the changes in GI that were attributed to a spawning event reflects a loss of gonadal tissue rather than an increase in gut fullness or fluid content. Without assessing this relationship, the use of GI to estimate the timing of spawning events in urchin populations may lead to erroneous inferences (Spirlet et al. 1998). In addition, changes in gonad weight also are a reflection of changes in the composition of gonadal tissue (i.e., nutritive phagocytes or gametes--see Harrington et al. 2007) that could be observed via histology. Another way to assess spawning is to examine the relative difference in mean gonad wet weight over the two successive sampling dates, immediately before and after spawning. The data for all sites combined revealed a drop in mean gonad weight of 61.1 % over that period (range = 45.1 %-76.7%). Similar observations were noted in other studies with Strongylocentrotus droebachiensis (Harrington et al. 2007) and with other sea urchin species (Drummond 1995).

Relationship between TD and GI

The relationship between TD and GI can influence estimates of reproductive condition. A number of biologists recognized earlier that a relationship existed between these variables (Fuji 1967. Pearse 1970). Fuji (1960b) and Moore (1963 a, 1963b) were among the earliest investigators to demonstrate a positive relationship between urchin size and GV or mass. Gonor (1972) critically analyzed the GI-TD relationship in Strongylocentrotus purpuratus and showed that for small urchins (<40 mm) GI varied directly with TD. This relationship is important because including animals below a species-specific minimum threshold size could bias estimates of GI and inferences about spawning. Before 2000, 45 of 105 studies (42.8%; Table 7) recognized the relationship between GI and TD, whereas since 2000, 77.4% of studies (48 of 62) used animals above a threshold minimum to assess spawning. Here, it was determined that an overall (nine sites) threshold size of 64 mm, above which, GI and TD were independent.

Two approaches have emerged to assess spatial or temporal changes in reproductive output. Both recognize an allometric relationship between TD (body size) and total weight, gonad weight, mass or GI that is a general phenomenon in marine invertebrates (McKinney et al. 2004, Hemachandra & Thippeswamy 2008) and sea urchins in particular (Gonor 1972, Lozano et al. 1995, Russell 1998, Muthiga 2005). The first involves a size-independent estimate of GI that uses information from the larger (mature) individuals in a population (Gonor 1972, Falk-Peterson & Lonning 1983, Brewin et al. 2000, Lamare et al. 2002) that may be site-specific (Sanchez-Espafia et al. 2004). Below a certain threshold TD, GI increases directly with body size (Fig. 3, Ebert et al. 2011). In Newfoundland, Keats et al. (1984a) saw no relationship between TD and GI for Strongylocentrotus droebachiensis between 20 and 50 mm. Comparisons of mean GI between sample dates and/or sites using ANOVA or other statistical tests assume that the gonad-to-body size ratio is consistent throughout the population (e.g., Himmelman 1978, Brady & Scheibling 2006). Use of urchins below the threshold size would bias estimates toward lower GI values. Three sites chosen deliberately to reflect smaller individuals (Fig. 4) showed no significant difference in mean GI through time for data using a restricted (i.e., [greater than or equal to] 64 mm TD) versus a complete size range (34.1-89.4 mm). It is likely that this lack of a significant difference reflects the large variability in the GI versus TD relationship for the >1,500 urchins sampled (Fig. 3).

The second approach (Grant & Tyler 1983, Packard & Boardman 1999) does not use size-specific indices such as GI, but relies on measuring a physiological variable, such as gonad weight, over the entire range of sizes of individuals in the population. Regression analysis followed by ANCOVA was used to remove the effects of body size allowing spatial and/or temporal comparisons of adjusted means (Ebert et al. 2011). If slopes of lines relating the physiological variable such as gonad weight are homogenous then ANCOVA can be used to compare adjusted means between monthly samples (Harrington et al. 2007) or between locations. This approach was used here to compare adjusted mean gonad weights, which supported earlier interpretations regarding site- and region-specific reproductive cycles made on unadjusted mean GI data (Fig. 8).

Causes of Variability

The geographic spread and diversity of bottom habitats of study sites (Table 1) allows for speculation on the possible causes of the observed variability in reproductive cycles. Mechanisms that trigger spawning are not well understood (Lamare & Stewart 1998, Oganesyan 1998). Both correlative and experimental approaches have been used to investigate spawning triggers in echinoids (Himmelman 1975, 1978, Levitan 1988a, Starr et al. 1990, Wahle & Peckham 1999, Gaudette et al. 2006). Several biotic and abiotic factors have been associated with spawning, including feeding/diets, habitat, water motion, intraspecific density, temperature, salinity, lunar phase, termination of the polar night, water depth, phytoplankton abundance, presence of gametes or pheromones, and temperature-dependent embryogenesis (Fujisawa 1989, Starr et al. 1993. Lamare & Stewart 1998, Oganesyan 1998, Himmelman 1999). Here, changes in GI were correlated with several of these factors.

Seawater temperature has long been cited to explain seasonal reproductive patterns in temperate urchins (Elmhirst 1923, Stott 1931. Bennett & Giese 1955, Fuji 1960b, Stephens 1972, Byrne 1990, Oyarzun et al. 1999, Brady & Scheibling 2006, but see Gonor 1973a, Himmelman 1978). Spawning in some tropical and subtropical urchins has been shown to vary with seawater temperature as well. Muthiga and Jaccarini (2005) showed that mean monthly GI in Echinometra mathaei in three Kenyan reef lagoons was positively correlated with mean monthly seawater temperatures ([r.sup.2] = 0.75). Similarly, Vai'tilingon et al. (2005) showed GI was negatively correlated with seawater temperature ([r.sup.2] = 0.20) for Tripneustes gratilla in the southern Indian Ocean. Seawater temperature explained 56% of the variation in GI over 12 mo for Lytechinus variegatus at one of four sampling stations near Miami, FL (Ernest & Blake 1981). Hernandez et al. (2006) and Tuason and Gomez (1979) reported the existence of a clear seasonality in the GI of Diadema antillarum (Canary Islands), and T. gratilla (near Mindoro Island, Philippines). The data presented here for Strongylocentrotus droebachiensis showed that mean seawater temperature explained between 55% and 77% of the variation in mean GI (Fig. 9). This does not imply that seawater temperature is a spawning trigger because the photoperiod cue and the temperature cue (decrease) occur simultaneously. Rather, the relatively high coefficient of determination can be used as a predictive tool (sensu Low-Decarie et al. 2014) to assess the timing of spawning in green urchins. Several authors have downplayed the role of temperature as a spawning cue (Himmelman 1978, Bayed et al. 2005, Scheibling & Hatcher 2001). Himmelman (1999) indicated that support for a "temperature hypothesis" is weak because few studies have examined alternative environmental factors.

Variation in diet has been associated with concomitant responses in GI in both the laboratory and field (Larson et al. 1980, Keats et al. 1983, Minor & Scheibling 1997, Meidel & Scheibling 1998, Vadas et al. 2000, James et al. 2007). Shallow-water habitats at most sites were dominated by crustose coralline barrens and filamentous algae. Patches of opportunistic macroalgae and refugiai kelp reflect high, preharvest urchin densities (Table 1). Diets of urchins mirrored barren-dominated habitats where benthic diatoms and filamentous microalgae were the abundant prey items at all sites for each season (Table 6). Others working in similar habitats have indicated the presence of diatoms in sea urchin diets (Vadas & Grant 1973, Chapman 1981, Duggins 1981). Generally kelps, which are among the more preferred prey in the diets of green urchins (Larson et al. 1980, Keats et al. 1984b, Lemire & Himmelman 1996), were absent or rare at most of our sites. The relatively minor differences in diet within and between regions through time (Table 6) cannot explain the significant spatial and temporal variation in GI.

Increases in intraspecific density of tropical and temperate sea urchins can result in reduced fecundity (Levitan 1989, Guillou & Lumingas 1998, Muthiga & Jaccarini 2005). Sea urchin densities at most of our study sites were relatively high (Table 1) and compare favorably with barren ground density estimates for this species in other northwestern Atlantic locations (Breen & Mann 1976, Scheibling & Hennigar 1997). For example, at shallow sites in the Gulf of Maine, Wahle and Peckham (1999) found a 50% decline in urchin (Strongylocentrotus droebachiensis) GI over a range of population densities from 0.1 to 250 ind./[m.sup.2]. To determine whether a relationship existed between the density of green urchins at the study sites (May to June 1988, Table 1) and maximum GI (typically March to May 1988, see Figs. 5-7), these two variables were regressed for all sites except Owl's Head, where no density measurements were taken and found no relationship (F = 0.56, df = 1,6, P = 0.48). Thus, over the range observed in this study, density did not show an expected inverse relationship with GI (sensu Levitan 1988b, Worthington & Blount 2003 as cited in Hill et al. 2003). Perhaps the lack of a significant relationship is the result of extensive barren habitats at our sites. Spawning in some sea urchins (e.g., Strongylocentrotus spp.) has been shown to correlate indirectly with seasonal increases in salinity (Starr et al. 1993, Vaschenko et al. 2001). We also examined the relationship between mean GI and salinity for all sites and sampling dates, and found no significant correlation between these variables (F = 0.75, df = 1, 57, P = 0.389, [r.sup.2] = 0.013; see Figs. 5-7).

In recent decades, seasonal phytoplankton blooms, along with their metabolites, have been considered as spawning cues in green and pale sea urchins (Himmelman 1978, Starr et al. 1990, 1992, Viktorovskaya & Zuenko 2005, Gaudette et al. 2006). This implies that larvae and phytoplankton abundance are closely synchronized (Thorson 1950), and that having urchin larvae in the water column concomitant with high concentrations of microalgae represents an evolutionary strategy (Himmelman 1999, Scheibling & Hatcher 2001). Others have reported similar findings with other urchin species. For example, Lopez et al. (1998) and Gonzalez-Irusta et al. (2010) showed that variations in larval abundance of Paracentrotus lividus from the northeast coast of Spain correlated closely with chlorophyll a concentrations. Muthiga and Jaccarini (2005) demonstrated that peak spawning activity in Eehinometra mathaei coincided with a peak in phytoplankton abundance. Spawning in other echinoderms (e.g., Cucumariafrondosa, Ophionotus victoriae) has been correlated with increasing concentrations of chlorophyll a (Hamel & Mercier 1995, Grange et al. 2004).

The perception that a particular variable induces spawning is not straightforward. Often, two or more variables appear to be correlated. For example, the distinction between temperature and chlorophyll a acting as an inducer for spawning is ambiguous because several field studies in arctic, temperate, and tropical waters have shown that the two variables are autocorrelated (Piatt et al. 1970. Bisagni et al. 1996, Stanwell-Smith & Peck 1998, McGillicuddy et al. 2001, Grange et al. 2004). Seward (2002) found that phytoplankton blooms in eastern Maine were correlated with many oceanographic variables including seawater temperatures, chlorophyll a, pheophytin, nitrate + nitrite, silicate, and phosphate. This suggests that a suite of variables may be responsible in the field for stimulating spawning in green sea urchins.

Also, spawning in sea urchins could be related more to thermal dependence of embryogenesis than other variables. Three species of cold- to warm-temperate urchins coexist on the Pacific coast of Japan near Kanagawa Prefecture (Fujisawa 1989), yet each species spawns during a different season. Although different species of phytoplankton may induce spawning during these seasons, an alternative hypothesis is that seawater temperature and/or photoperiod (sensu Kelly 2000) induces gametogenesis. Walker and Lesser (1998) showed that ovaries of animals exposed to a photoperiod advanced by 4 mo were significantly larger by as much as 175% than control (field) animals mostly due to accelerated development of nutritive phagocytes. New, vitellogenic primary oocytes occupied <1% of the volume fraction of the gonads compared with nutritive phagocytes (ca. 90%). Fujisawa and Shigei (1990) demonstrated that optimum temperature range for development in eight species of temperate and tropical sea urchins was closely related to seawater temperatures during the spawning season. The results suggest that gametes are shed during times when seawater temperature is increasing from ca. 1-7[degrees]C (Figs. 5-7), which corresponds to optimum embryo and larval development in Strongylocentrotus droebachiensis (Stephens 1972).

Assessment of Spawning

Early attempts to assess spawning (e.g., Fox 1922, Elmhirst 1923) were qualitative, usually graphical presentations. A progression of techniques has followed including direct observations in the field, gonadal smears, changes in GI, gonadal weight, or volume through time, microscopy, and histology (Fuji 1967, Pearse 1968, Keatsetal. 1987, Youngetal. 1992, Kinget al. 1994, Viktorovskaya & Matveev 2000, Brady & Scheibling 2006, Sellem & Guillou 2007, Pecorino et al. 2013, Wangensteen et al. 2013, see Table 7). Moore (1934) was the first to use GI to assess spawning in urchins. Of 167 papers published between 1922 and 2013 in which methods of spawning in wild populations of regular sea urchins (species number = 54) were described (Table 7), 84 (50.2%) and 134 (80.2%) used histology and GI, respectively.

Here, spawning was assessed by analyzing changes in GI through time rather than examining gonads histologically. The use of both histology and GI to assess spawning has increased in recent years. Histology can demonstrate whether ovaries contain large percentages of nutritive phagocytes (prespawning), mature ooyctes (spawning is imminent), and relict oocytes (partly spawned to spent). Interestingly, there may be considerable variation in spawning associated with the number of mature oocytes. For example, King et al. (1994), indicated that mature oocytes are not necessarily released at initial maturity but can be held within the test indefinitely. Also, "the temporal pattern in the gametogenic index of females was similar across depth strata and concordant with the pattern in gonad index" (Brady & Scheibling 2006). In a few species, however, only weak correlations existed between GI and histological condition of the gonad, [e.g., Centrostephanous rodgersii (King et al. 1994) and Heliocidaris species (Laegdsgaard et al. 1991)].

Generally, there is good concordance between GI and histology. Harrington et al. (2007) examined stereologically nutritive phagocytes and gametogenic cells during the annual reproductive cycle of Strongylocentrotus droebachiensis, and stated that GI serves as a good assessment of the seasonal reproduction cycle. The histology of the gonads of two tropical species (Diadema setosum and Echinometra mathaei) was correlated with GI and was similar to that of other urchins (Alsaffar & Lone 2000). Bigatti et al. (2004) indicated that GI in Pseudechinus magellanicus appeared to be a good indicator of the reproductive cycle, corroborated by gonad histology. Byrne (1990) and King et al. (1994) also verified spawning times by the histological condition of the gonads. Ourens et al. 2011, concluded that histology was the most reliable tool for determining the reproductive cycle of Paracentrotus lividus.

Mature gametes, however, are not necessarily an indication of spawning (Mahdavi Shahri et al. 2008). The presence of ripe gonads with mature gametes only indicates a readiness to spawn given the right cue. Spawning may not occur until the animal experiences certain cues or stimuli (Byrne 1990, Starr et al. 1990. Byrne et al. 1998). Where both GI and histological data have been reported, maximum gonad size usually corresponds to periods when highest percentages of ripe individuals occur in collections (e.g., McPherson 1965--Tripneustes ventricosus; Dix 1970--Evechinus chloroiicus; Gonor 1973a--Strongylocentrotus purpuratus), (see Ernest & Blake 1981). Furthermore, for Centrostephanus rodgersii near the Solitary Islands, New South Wales, Australia, histological examination confirmed that maximum spawning activity was in August (winter) (O'Connor et al. 1978) and the GI figure (Fig. 1, p. 2) shows a major decline in GI between the July and August (1973-1974) sampling dates.

Gonad Index: Assumptions, Calculations, and Statistics

Surprisingly, 19 different techniques and/or formulae have been used for calculating GI in echinoids (Table 7; see Table 8 for a subset of comparisons of these formulas applied to data from sites selected from each region in this study). Also, Ebert et al. (2011) described multiple ways GI was calculated for echinoids and other echinoderms. Earlier, Spirlet et al. 1998 argued for the inclusion of both the GI and maturity index (histological data on the change from nutritive cell to gametogenic cells). Historically, GI measures have changed from volumetric to mass based. Before 1970, 21 of 25 papers used volumetric measures to calculate GI. Kelly (2000) refined techniques for estimating GI by eviscerating the test and removing food items, sediments, etc. from the test before weighing and calculating the index. Previous indices may have been too conservative because of the presence of these items in the test before weighing the roe. Since 1989, the trend has been to use a GI similar to the one used in this study (57.6%, or 49 of 85 papers). Overall, the use of GI to assess spawning has increased over time (G-statistic = 23.82, df = 4; P < 0.0001). Before 1970, 48% of papers used this metric, however, since 2000 GI has been used nearly 95% (59 of 62) of the time. Before 2000, 37 of 105 papers (ca. 35%) used both GI and histology, whereas after 2000, the rate was 33 of 61 papers (54%) (Table 7). Recently there has been an emphasis on the need to standardize the methodology for calculating GI (Ebert et al. 2011, Ourens et al. 2012, 2013).

Many of the qualitative estimates used to assess spawning that are described in Table 7 included means [+ or -] a measure of error (e.g., SE, SD, 95% CI), but no statistical analyses (i.e., hypothesis tests) were conducted. On the other hand, quantitative assessment of reproductive cycles has become more common in recent decades. To the best of our knowledge, the first attempt to quantify statistically the timing of spawning in sea urchins was by Pearse (1969a) who used ANOVA to detect differences in mean GI in Prionocidaris baculosa from the Gulf of Suez. It is not clear, however, how results from the ANOVA were interpreted. That is, whether an overall F-statistic and its P value were used to assess variability over an annual cycle or, if a series of F-statistics were used to compare discrete periods (usually monthly) of time within the annual cycle (e.g., March versus April or May and June versus July). For example, a significant F-value for a set of monthly GI means (temporal variability) does not give precise information about when spawning occurred. Instead, a posteriori tests (e.g., SNK, Tukey, Scheffe) or a series of a priori contrasts should be used to further draw out the information about specific temporal patterns. Here, ANOVA was used to determine spatial and temporal variation in mean GI and preplanned orthogonal contrasts to delineate spawning within the annual cycle. In addition, there has been a trend to use statistical methods to assess spawning over time (Table 7). Before 2000, 11 of 105 papers (ca. 10%) used a statistical test to determine when spawning occurred. Since then, 34 of 62 papers (ca. 55%) have used these techniques.

Maine Management Plan

Green sea urchins have been harvested commercially in Maine, United States, because landings have been recorded (1964, 55 mt) (DMR 2014). A large-scale fishery developed subsequent to the sampling conducted in 1987. Peak landings occurred in 1993 (18,800 mt, worth $26.8 million); however, by 1997, landings fell below 10.000 mt, and. by 2012, had declined to precommercial levels at 863 mt (DMR 2014). Currently, the DMR management plan focuses on four major harvesting constraints. The first is based on perceived regional differences in the timing of reproduction that is denoted by a line near mid-coast that divides the state into two management zones. "Zone 1" extends from the Maine/New Hampshire boarder to the mouth of the Penobscot River. "Zone 2" continues from the off-shore islands in Penobscot Bay to the Canadian border (see Fig. 2 in Chen & Hunter 2003). A person may hold a license from only one zone. The second constraint relates to urchin reproductive cycles within each zone that sets the harvest seasons. The third and fourth address limited entry and minimum and maximum size limits, respectively. The zones reflect inherent differences in seawater temperatures and nutrients between the two regions (Townsend et al. 2010), and because this study found that between 55% and 77% of the variation in mean GI can be explained by seawater temperature, it would appear that continued use of these zones is justified. Four of the nine sites in this study are in Zone 1, with spawning at each occurring between April and May (Figs. 56). Spawning at the remaining five sites was more variable temporally (Figs. 6-7). Also, the interannual variability shown by a comparison with earlier and later urchin studies in Maine (Cocanour & Allen 1967--Lamoine, Gaudette et al. 2006--Boothbay Harbor) attests to the extreme variability in spawning along the coast of Maine. Because of the large variability observed in GI both within and between sampling sites, and interannually within a subset of the sampling sites through time (Cocanour & Allen 1967, Seward 2002, Gaudette et al. 2006), potential differences in reproduction and spawning (even if not so subtle) were unable to be discerned, and limits the refinement of current management practices in Maine.

Gonad Index and a HW

Because GI is a relative measure of reproduction (timing and effort), it is readily subject to differing views and interpretations (Ebert et al. 2011, Ourenset al. 2012). It would be desirable to standardize the measure of GI so that researchers. resource managers, and commercial enterprises have a common reference and understanding of what the results mean. To this end, Ebert et al. (2011) (using gonad wet weight) and Ourens et al. (2012) (using gonad dry weight) both developed allometric models to calculate GI. A detailed understanding of spawning cycles, especially possible triggers (Kirchhoff et al. 2010) and duration (Byrne et al. 1998), would provide the basis for developing specific models for identification of what is termed here as "harvest windows". These windows (based on location-specific GI, e.g., estuaries, bays, inlets, lagoons, and islands) represent segments of time (days, weeks, months, etc.) during the general spawning season when GI are at or above 10% (e.g., see Fig. 4. Schoodic Point) (10% represents the minimal commercial standard in Maine (Vadas et al. 2000). By focusing on initiation of harvesting at 10% and termination at the first signs of "melt" (wide-spread) release of gametes from goniducts on the aboral surface), the windows would retain (conserve) a residual population of small urchins for further growth and large urchins for breeding stock. These windows could be adjusted by increasing or decreasing GI values to enhance sustainability and conservation efforts. Ourens et al. (2011) concluded that understanding the reproductive cycle would provide a tool (guide) for management, allowing sea urchins to spawn several times during their life span before being harvested. The concept of HW would be a refinement of this management tool.

A typical cycle for Strongylocentrotus droebachiensis in Maine would include "prematuration" (fall development of roe contents and gonad growth), "maturation" (winter), "spawning and melt" (spring) and "recovery" (summer) (see also Byrne 1990, Harrington et al. 2007). Unless tested statistically, the small peaks and downturns in GI (fractional spawning) should be considered as sampling noise. A statistical approach for identifying and analyzing these events may permit the development of predictive relationships at local scales. Such predictors may enhance the analysis of multiple factors (different salinities, foods, temperatures, etc.) and therefore provide greater insight for determining when to set the initiation and termination points of HW. Detecting the termination phase (as soon as melting is recognized at the site) will be difficult because of the wide variability in spawning (as shown here). Such information will permit the integration of predictions into management strategies to provide better estimates of marketing and conservation of immature urchins with little roe and legal sized urchins with melted roe, respectively. The search for appropriate HW may provide another tool for harvesting and sustaining urchin populations with quality roe.

ACKNOWLEDGMENTS

We greatly appreciate the interactions and diving assistance of Bruce Chamberlain (Maine Department of Marine Resources) and Ben Baxter (formerly of Maine Cooperative Extension). We thank Dr. Michael Lesser for critically reviewing the manuscript. We appreciate the reference work of Dennis Anderson and Shannon Alexa. We gratefully acknowledge the funding and related support from the NOAA Maine Sea Grant program, the University of Maine Cooperative Extension, the Maine Department of Marine Resources, and the Maine Agricultural and Forest Experiment Station (contribution no. 3431).

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ROBERT L. VADAS, Sr., (1,2) * BRIAN F. BEAL, (3) STEVEN R. DUDGEON (1,4) AND WESLEY A. WRIGHT (1)

(1) School of Biology and Ecology, University of Maine, 7 Grove Street Extension, Orono, ME 04469; (2) School of Marine Sciences, University of Maine, Orono, ME 04469; (3) Division of Environmental and Biological Sciences, University of Maine at Machias, 116 O'Brien Avenue, Machias, ME 04654; (4) Department of Biology, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330

* Corresponding author. E-mail: vadas@maine.edu

DOI: 10.2983/035.034.0337

TABLE 1.
Description of nine study sites, covering a distance of 270 km, and
mean density in 0.25 [m.sup.2] quadrats (mean number of individuals
per 1 [m.sup.2] [+ or -] 95% CI in May to June 1988) of
Strongylocentrotus droebachiensis in three coastal regions of Maine.

Region   Site *        Latitude            Longitude

SW        BYI     43[degrees]43'06"    70[degrees]00'16"
          FVI     43[degrees]49'43"    69[degrees]42'57"
          BBH     43[degrees]48'91"    69[degrees]35'72"
CN        OWH     44[degrees]05'55"    69[degrees]03'49"
          STN     44[degrees]09'15"    68[degrees]41'45"
                          --                  --
          LMB     44[degrees]27'21"    68[degrees]16'81"
NE        SPT     44[degrees]20'27"    68[degrees]02'72"
                          --                  --
                          --                  --
          JPT     44[degrees]32'36"    67[degrees]33'69"
          LBC     44[degrees]48'45"    66[degrees]58'62"

Region   Site *        Inhabits         Depth range (M)

SW        BYI        BK ([dagger])            2-3
          FVI     B ([double dagger])         2-3
          BBH              B                  2-3
CN        OWH              B                  2-3
          STN              B                  2-3
                          --                  4-7
          LMB              B                  2-3
NE        SPT      BK ([paragraph])           2-3
                          --                  4-5
                          --                  6-8
          JPT      BK ([paragraph])           1-3
          LBC      BK ([paragraph])           2-5

Region   Site *         N          Mean   95% CI

SW        BYI           12         68.8    42.9
          FVI           12         39.5    17.2
          BBH           12         43.8    23.7
CN        OWH     ND ([section])    --      --
          STN           10         5.0     7.5
                        10         5.0     7.5
          LMB           10         30.0    12.0
NE        SPT           8          0.0     0.0
                        8          28.0    8.0
                        8          13.0    10.9
          JPT           19         1.3     2.8
          LBC           12         20.8    18.9

SW, southwest; CN, central; NE, northeast; BYI, Bailey Island; FVI.
Five Islands; BBH. Boothbay Harbor; OWH, Owl's Head; STN, Stonington;
LMB, Lamoine; SPT. Schoodic Point; JPT, Jonesport; LBC. Lubec.

* Sites ordered from southwest to northeast,

([dagger]) Barrens with scattered, refugial kelp,

([double dagger]) Barrens.

([section]) No quantitative data; seasonally there was a bloom of
green algae, but the yearly pattern was a barren.

([paragraph]) Kelp shallow; barrens deeper.

TABLE 2.
Lack-of-fit analysis and allometric model results for the
relationship between urchin TD and GI.

                         Lack-of-fit analysis

                           Linear                Quadratic

                             P       [r.sup.2]       P       [r.sup.2]

All data (n = 1,594)      <0.0001#    0.1030     <0.0001#     0.1138
[greater than or equal    <0.0001#    0.0923     <0.0001#     0.1090
  to]45 mm (n = 1,553)
[greater than or equal    <0.0001#    0.0661     <0.0001#     0.0867
  to]50 mm (n = 1,480)
[greater than or equal    <0.0001#    0.0255      0.0002#     0.0354
  to]55 mm (n = 1,348)
[greater than or equal    0.0029#     0.0078      0.0201#     0.0125
  to]60 mm (n = 1,139)
[greater than or equal     0.0851     0.0031      0.0359#     0.0078
  to]62.5 mm (n = 943)
[greater than or equal     0.2978     0.0013      0.0714      0.0052
 to]64 mm (n = 834)

                         Lack-of-fit analysis

                           Cubic                Allometric

                             P      [r.sup.2]       P        [r.sup.2]

All data (n = 1,594)      0.0009#    0.1200      <0.0001#     0.1437
[greater than or equal    0.1251     0.1103      <0.0001#     0.1308
  to]45 mm (n = 1,553)
[greater than or equal    0.9621     0.0868      <0.0001#     0.0863
  to]50 mm (n = 1,480)
[greater than or equal    0.8848     0.0354      <0.0001#     0.0268
  to]55 mm (n = 1,348)
[greater than or equal    0.7899     0.0125      0.0056#      0.0067
  to]60 mm (n = 1,139)
[greater than or equal    0.7283     0.0079       0.0749      0.0034
  to]62.5 mm (n = 943)
[greater than or equal    0.6533     0.0055       0.2691      0.0015
 to]64 mm (n = 834)

Overall TD for complete data set ranged from 34.1 to 89.4 mm.
Significant P values are shown in boldface.

Note: Significant P values are indicated with #.

TABLE 3.
Mean GI ([+ or -] 95% CI) and mean percent loss of GI for each region
and site for the month before and after spawning.

Region   Site   n      Prespawn     n     Postspawn    Percent loss

SW       BYI    12   18.4 (10.1%)   12   9.0 (2.3%)              51.1
         FVI    15   17.4 (6.2%)    15   8.3 (3.5%)              52.3
         BBH    12   22.7 (10.8%)   12   7.9 (3.3%)              64.8
                                                       [bar.x] = 55.8
CN       OWH    13   13.1 (4.8%)    13   5.9 (1.3%)              54.9
         STN    15   17.6 (7.2%)    15   3.9 (1.6%)              77.8
         LMB    15   9.1 (8.2%)     15   3.4 (2.4%)              62.6
                                                       [bar.x] = 65.6
NE       SPT    15   20.0 (8.6%)    15   9.2 (4.7%)              54.0
         JPT    13   15.4 (7.7%)    13   6.9 (3.6%)              55.2
         LBC    12   19.9 (6.6%)    12   10.4 (5.9%)             47.7
                                                       [bar.x] = 52.5

                                          Overall [bar.x] = 58.2

SW, southwest; CN, central; NE, northeast; BYI, Bailey Island; FVI,
Five Islands; BBH, Boothbay Harbor; OWH, Owl's Head; STN, Stonington;
LMB, Lamoine; SPT, Schoodic Point; JPT. Jonesport; LBC, Lubec.

n = number of urchins sampled on each date-see Figs. 5-7.

TABLE 4.
Summary of single-factor ANOVA results.

                          Complete data

                           Contrasts *

Site   df      1          2                3

BYI    12   <0.0001#   0.2549     0.0645
FVI    12   <0.0001#   0.0002#    0.2467
BBH    12   <0.0001#   0.0006#    0.0239
OWH    11   <0.0001#   0.4069     0.0082#
STN    11   <0.0001#   <0.0001#   0.4652
LMB    11   0.0003#    0.0046#    0.9946
SPT    11   <0.0001#   0.1983     0.0723
JPT    10   <0.0001#   0.3481     0.0001# ([section])
LBC    10   <0.0001#   0.9108     0.8748

       >64 mm

                      Contrasts ([dagger])

Site            1               2               3

BYI    <0.0001#               0.2687   0.0470
FVI    0.2387                 0.9122   0.3253
BBH    <0.0001#               0.0220   0.0465
OWH    <0.0001#               0.0992   0.3607
STN    0.0002#                0.1919   0.9360
LMB    -- ([double dagger])   --       --
SPT    <0.0001#               0.1578   0.2927
JPT    0.0002#                0.3583   0.0003# ([section])
LBC    <0.0001#               0.8230   0.2526

BYI, Bailey Island; FVI, Five Islands; BBH, Boothbay Harbor; OWH,
Owl's Head; STN, Stonington; LMB, Lamoine; SPT, Schoodic Point;
JPT, Jonesport; LBC, Lubec.

Dependent variable: arcsine-transformed monthly GI data for green sea
urchins at each of nine sites along the Maine coast from September
1987 to 1988. Independent variable: month (10-14dates per site). Four
single degree-of-freedom, a priori contrasts were conducted for each
ANOVA. To control for excessive type I error, a decision rule of
[alpha]' = 0.0127 was used (Winer et al. 1991). Boldface P values are
statistically significant. 6 [less than or equal to] n [less than or
equal to] 15.

* Contrast 1: January, February, March, April versus May, June, July;
contrast 2: January, February, March versus April; contrast 3: May
versus June, July; contrast 4 (not shown): July versus August,
September (no contrast was significant, P > 0.0127). Analyses were
performed using complete size range of urchins (34.1-89.4 mm),

([dagger]) Analyses performed on urchins with TD [greater than or
equal to] 64 mm.

([double dagger]) All urchins had TD < 64 mm at Lamoine.

([section]) Postspawning recovery contrast = June versus July, August,
September (see Figure 7).

Note: P values are statistically significant are indicated with #.

TABLE 5.
Analysis of variance on the arcsine-transformed mean maximum
GI for nine sites and three regions of the Maine coast.

Source of variation   df    SS        MS       F       Pr > f

Region                  2    919.66   459.83   18.01   <0.0001#
Site (Region)           6    665.44   110.91    4.34    0.0006#
SW region               2    111.00    55.50    2.17    0.1189
CN region               2    492.36   246.18    9.64    0.0001#
NE region               2     62.08    31.04    1.22    0.2991
Error                 113   2885.39    25.53
Total                 121   4470.50

SW, southwest; CN, central; NE, northeast.

Maximum values for GI occurred between February and April 1988. To
control for excessive type I error, a decision rule of [alpha]' =
0.0170 was used (Winer et al. 1991). Boldface P values are
statistically significant. 12 [less than or equal to] n [less than
or equal to] 15.

Note: P values are statistically significant are indicated with #.

TABLE 6.
Relative seasonal abundance of five algal functional groups in
the gut of green sea urchins within three regions of the coast of
Maine.

              Functional
                 algal                       Region

Season          Groups      Southwestern     Central     Northeastern

Late fall     Diatoms       X              XXXX          XXX
              Microalgae    XXX            XXXX          XX
              Filamentous   XX             XXXXX         X
              Foliose       X              XX            XX
              Macrophytes   X              XX            XX
              Relative      1 2 3 4 5 6    1 2 3 4 5 6   1 2 3 4 5 6
                abundance
Late winter   Diatoms       XX             XXXX          XXX
              Microalgae    xxxx           XX            XXXXX
              Filamentous   X              XXX           X
              Foliose       XX             XX            XX
              Macrophytes   XX             X             XX
              Relative      1 2 3 4 5 6    1 2 3 4 5 6   1 2 3 4 5 6
              abundance
Spring        Diatoms       XX             XXX           XXXXX
              Microalgae    XX             XXXX          XX
              Filamentous   XX             XXXX          XXXX
              Foliose       XX             XX            XX
              Macrophytes   XX             XX            XX
              Relative      1 2 3 4 5 6    1 2 3 4 5 6   1 2 3 4 5 6
              abundance
Summer        Diatoms       XXX            XXXX          XX
              Microalgae    XX             XXX           X
              Filamentous   XX             XXXX          XX
              Foliose       XX             XX            X
              Macrophytes   X              X             X
              Relative      1 2 3 4 5 6    1 2 3 4 5 6   1 2 3 4 5 6
              abundance

Summary data are presented from three sites within each coastal region
(see Table 1). The gut of five randomly chosen urchins was dissected
seasonally from each site. 1 = absent, 2 = rare, 3 = infrequent, 4 =
present, 5 = common, 6 = abundant (e.g., relative abundance of diatoms
in the central region during the late fall ranged from rare to common;
macrophytes in the northeastern region during summer were absent).

TABLE 7.
Methods of assessing spawning in wild populations of regular sea
urchins. (Taxonomy after World Register of Marine Species,
www.marinespeeies.org).

                                                       Relationship
How spawning                   Urchin size             between GI *
was assessed                    (mm or g)             and TD * (mm)

Direct observation                 nd                       x
Extrusion of ripe                  nd                       x
  ova; appearance of
  larvae and early
  juveniles
Fertilization trials               nd                       X
Observation of spent               nd                       X
  individuals
  ([dagger])
  microscopy
GI ([double dagger]);              nd                No relationship
  microscopy                                          between TD and
                                                        gonad size
Direct observation of           12.5-57.5          Gonad volume linear
  gonad releasing                                  f(x) of test volume
  gametes;
  microscopy;
  histology
Sperm agglutination                nd                       X
  tests both species               nd                       X
GI ([section])                     nd                       X
GI [+ or -] 95% CI                 nd                       X
  ([section])
GI [+ or -] 95% CI                 nd                       X
  ([section])
Visual assessment of               nd                       X
  gonad ripeness
GI distribution plots              nd                       X
  ([section])
GI ([paragraph]);                  nd                       X
  plankton tows for
  larvae
GI ([section])                     nd                       X
GI ([section]);                   55-96                     XO
  fertilization
  studies
GI [+ or -] 95% CI                 nd                       X
  ([section])
GI [+ or -] SE                >40 for both                  XO
  ([parallel]);                  species                    XO
  histology for both
  species
GI ([double dagger])               >40              Gonad volume is an
                                                   allometric function
                                                          of TD
GI ([double dagger])               >50              Gonad volume is an
                                                   allometric function
                                                          of TD
GI [+ or -] SD                  146-715 g                   X
  ([section])
Direct observation                32-67                     X
GI [+ or -] SD                     nd                       X
GI ([double dagger]);              >50                      XO
  microscopy
GI ([section])                     nd                       X
GI [+ or -] 95% CI                 nd                       X
  ([section])
GI ([paragraph];                   nd                       X
  microscopy
GI [+ or -] SE                    50-70                     XO
  ([section])
GI [+ or -] SE                     >40              Gonad volume is an
  ([parallel]);                                    allometric function
  microscopy                                              of TD
Histology                        10-40 g                    X
GI ([double dagger]);          (18-110 ml)                  XO
  microscopy; KC1
  injection
GI [+ or -] 95% CI                 nd                       X
  ([section]);                     nd                       X
  histology ; %                    nd                       X
  mature
GI [+ or -] 95% CI                8-39                    XX **
  ([double dagger]);
  microscopy;
  histology
Direct observation;               31-98                     XO
  histology                       32-81
Histology                         40-67                     XO

Histology                        6-10 g                     x
GI [+ or -] error                  nd                       X
  bars ([double                    nd                       X
  dagger]);                        nd                       X
  microscopy                       nd                       X

GI ([double dagger]);             25-65                     XO
  microscopy;                     25-65                     XO
  histology
GI [+ or -] SD;                   33-69                     XO
  ANOVA; direct
  observation;                    40-76                     XO
  histology
GI [+ or -] SD;                   40-69                     XO
  direct observation;
  histology
GI ([double dagger]);             45-81            Decrease in GI with
  microscopy                     95-150               increasing TD
GI [+ or -] SD;                   36-95                     XX
  histology
GI ([double dagger])               nd                       X
Microscopy; histology              nd                       X
  ([dagger])
  ([dagger])
GI; microscopy                   51-102                     X
  (proportion of ripe              nd                       X
  eggs from the
  population)
Histology                          >45                      XX
GI[+ or -] 95% CI                  >45                      XX
  ([double dagger])
  ([double dagger]);
  histology
Direct observation             0.9-47.3 g                   X
Percent of urchins                 nd                       X
  oozing gametes
GI [+ or -] 95% CI                45-70                     XX
  ([section])
  ([section])
Direct observation;                nd                       X
  GI [+ or -] 95% CI
Percent of urchins                 nd                       X
  oozing gametes;
  oocyte size-
  frequency
  distribution;
  histology
GI([double dagger]);               nd                       X
  histology
GI [+ or -] error                >100 mm           Linear relationship
  bars (undefined)                                        to 95
  ([paragraph])
  ([paragraph]);
  histology
GI [+ or -] SE;                    >60                      XX
  microscopy;
  histology
GI [+ or -] error                  nd                       X
  bars (undefined);
  microscopy;
  histology
GI ([paragraph])                   >40                      XX
  ([paragraph])
GI ([parallel])              [bar.x] = 70.7                 X
  ([parallel]);            (SD [+ or -] 1.59)
  histology
GI [+ or -] 95% CI;            >30 g for                    XX
  ANOVA (undefined a          each species                  XX
  posteriori test)                                          XX
GI [+ or -]2 SE                    nd                       X
  ([double dagger]);               nd                       X
  histology (for each              nd                       X
  species)                         Nd                       X
GI for both species;               nd                       X
  histology for T.                 nd                       X
  gratilla
GI                                 >30                      X
Histology for each                 nd                       X
  species                          nd                       X
                                   nd                       X
                                   nd                       X
                                   nd                       X
GI [+ or -] SE;                  30-110                     X
  histology
GI [+ or -] SD                    55-65                     XX
  ([double dagger])
  ([double dagger]);
  histology
Adjusted mean GI                   nd               Allometric between
  [+ or -] 95%                     nd               GI and body weight
  CI ***; microscopy               nd                for each species
  for all species                  nd
                                   nd
GI [+ or -] SD                     nd                       X
  ([double dagger]);
  histology; oocyte
  size-frequency
  distribution
Changes in adjusted                >40                      XX
  GV through time;
  histology
GI [+ or -] SD;                  ca. 60                     XX
  seawater-induced                                          XX
  gamete release;
  histology for both
  species
GI [+ or -]SE                     20-50               No significant
                                                       relationship
GI ([double dagger]);             8-70                      X
  microscopy
Oocyte size-frequency              nd                       XX
  distribution;
  histology
KC1 injection                      nd                       X
                                   nd                       X
                                   nd                       X
                                   nd                       X
                                   nd                       X
GI [+ or -] 95% CI                 nd                       XX
  ([dagger])([dagger])
  ([dagger]); oocyte
  size-frequency
  distribution;
  histology
Proportion of                      nd                       X
  population observed
  to be spawning
Direct observation;               20-85            XX ([double dagger])
  KC1 injection; [bar.x]                            ([double dagger])
  percent spawning                                  ([double dagger])
  [+ or -] SD
[bar.x] [+ or -] 95% CI            nd                       XX
  gonad dry weight
  through time; %
  mature gonads;
  microscopy
GI [+ or -] SD                    30-65                     XX
  ([double dagger])
  ([double dagger]):
  histology
GI [+ or -] SD;                    >40                      XX
  histology; KC1
  injection;
  microscopy
GI [+ or -] SE;                    nd                       X
  histology
GI [+ or -] SE                    55-80                     XX
  ([double dagger])               55-95                     XX
  ([double dagger]);
  ANOVA, SNK;
  histology
GI [+ or -] SE                    60-80              No relationship
                                                      after TD > 50
Microscopy; histology              nd                       X
GI [+ or -] SD;                   55-76                     XX
  histology
GI [+ or -] SD                    80-90                     XX
  ([section])
  ([section])
  ([section])
GI [+ or -] 95% CI;               40-60                     XX
  ANOVA, Scheffe's
  test; direct
  observation;
  microscopy
GI [+ or -] SD;                   55-76                     XX
  histology
GI [+ or -] 95% CI;                nd                       X
  histology                        nd
GI [+ or -] SD                    80-90                     XX
GI [+ or -] SE                   70-100                     XX
  ([double dagger])
  ([double dagger]);
  ANOVA, SNK test;
  KC1 injection;
  histology
GI                                45-95                     XX
GI [+ or -] SE; Mest;              nd                       X
  histology for both               nd                       X
  species
GI [+ or -] SE                     >30                      XX
  ([paragraph])
  ([paragraph])
  ([paragraph]);
  ANOVA, Tukey's
  test; histology
GI [+ or -] SE                   50-130+           No relationship at
  ([section]); ANOVA,                                northern sites;
  SNK test                                              quadratic
                                                   relationship found
                                                     at southern site
GI [+ or -] 95% CI                31-50                     XX
  ([parallel])
  ([parallel])
 ([parallel]); ANOVA,
  Tukey's HSD test
GI [+ or -] 95% CI;                >40                      XX
  histology
GI [+ or -] SE;                  66-120            No relationship from
  histology                                           66 to 119 ****
Seasonal changes in                >70                      X
  mean gonad dry
  weight
GI [+ or -] 95% CI                41-50                     XX
  ([parallel])
  ([parallel])
  ([parallel])
GI [+ or -] SD                    80-90                     XX
  ([section])
  ([section])
  ([section]);
  histology
GI [+ or -] SE                     nd                       X
  ([paragraph])
  ([paragraph]);
  direct observations
GI [+ or -] SE                     nd                       X
  ([paragraph])
  ([paragraph]);
  direct observations
GI [+ or -] SD;                   35-50              No relationship
  ANOVA; histology                                  between 35 and 50
GI [+ or -] 95% CI,               60-70                     XX
  histology
GI [+ or -] SD;                   35-50                     XX
  histology
KC1 injection; field               nd                       X
  observations of
  larvae
GI [+ or -] SD                   80-115                     XX
  ([section])
  ([section])
  ([section]);
  Wilcoxon-Mann-
  Whitney test
GI [+ or -] error            [greater than                  X
  bars (not defined);        or equal to]70
  histology
GI [+ or -] SE                27.9-105.1 g                  XX
  ([paragraph])                23.6-66.3 g
  ([paragraph]);
  ANOVA, SNK test;
  histology
GI ([dagger])                     35-45                     XX
  ([dagger])
  ([dagger])
  ([dagger]);
  microscopy; KC1
  injection
GI [+ or -] SE               [greater than           No relationship
  ([paragraph])              or equal to] 70          after TD > 70
  ([paragraph]);
  ANOVA; histology
GI [+ or -] SD                     >30                      XX
  ([double dagger]),
  ***
GI [+ or -]95% CI                 45-58                     XX
  ([parallel])
  ([parallel])
  ([parallel]);
  Kruskal- Wallis,
  SNK tests
GI [+ or -] 95% CI                20-30                     XX
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
  histology
GI ([parallel]);                   nd                       X
  histology
GI [+ or -] SE                     >40                      XX
  ([double dagger])
  ([double dagger])
GI [+ or -] SE                   70-140                     XX
  ([paragraph])
  ([paragraph]);
  ANOVA; histology
GI [+ or -] SD;                    nd                       X
  histology
GI [+ or -] SE                    30-60                     XX
  ([section])
  ([section])
  ([section])
  ([section]); ANOVA,
  Tukey's test; KC1
  injection; histology
GI [+ or -] 95% CI                 >12                      X
GI [+ or -] SD                  21.7-50.8                   X
                                44-80.8                     X
                              ([paragraph])
                              ([paragraph])
                              ([paragraph])
                              ([paragraph])
GI ****; Kruskal-                 40-60                     XX
  Wallis; histology
GI [+ or -] SD; ANOVA,             >20                      XX
  Tukey's test;
  histology
GI [+ or -] SD; ANOVA,         54.5-60.3                    XX
  Tukey's B test                (without
                                 spines)
GI [+ or -] SE; KC1           61.2 [+ or -]                 XX
  injection: histology          0.4 68.3
                               [+ or -]0.4
                              ([parallel])
                              ([parallel])
                              ([parallel])
                              ([parallel])
GI [+ or -] SE                    40-84                     XX
  ([paragraph])
  ([paragraph]),
  *****; histology
GI [+ or -] SD                     >30                      XX

GI [+ or -] SD;                    >12                      X
  histology
GI [+ or -] SE; ANOVA,             >20                      XX
  Tukey's test:
  histology
GI [+ or -] SD *****;              >40                      XX
  histology
GI [+ or -] SE                    30-35                     XX
  ([parallel])
  ([parallel])
  ([parallel]); ANOVA,
  Tukey's HSD test
GI [+ or -] SD                     nd                       X
  ([section])
  ([section])
  ([section])
  ([section]);
  microscopy (for each
  species)
GI [+ or -] SE: KC1               45-80               No significant
  injections;                                      relationship between
  histology                                             45 and 80
GI [+ or -] SE; ANOVA;            25-60                     X
  KC1 injections;
  histology
GI                           [greater than                  XX
                             or equal to] 22
GI [+ or -] SD; ANOVA;            70-90                     XX
  histology
GI [+ or -] SD; ANOVA;             >30                      XX
  Scheffe test;
  histology
GI [+ or -] SD;                   35-69               No significant
  ANOVA *****                                       relationship over
                                                        size range
GI [+ or -] SE; ANOVA,             nd                       X
  Fisher's LSD, Mann
  Whitney tests
GI [+ or -] SE ***;                nd                       X
  ANOVA(ns)
GI [+ or -] SD                    32-36                     XX
  ([section])                     22-25
  ([section])
  ([section]); ANOVA,
  LSD
GI [+ or -] SE;                 9.3-24.1                    XX
  histology; ANOVA on
  mean oocyte
  diameter, Tukey's
  test
GI [+ or -] SE;                    nd                       X
  ANOVA(ns); histology
Dry gonad mass                    28-33                     XX
  [+ or -] SE; KC1
  injection; histology
GI [+ or -] SD;                    >45                      XX
  Kruskal-Wallis,                  >26
  Tukey's tests;
  macroscopic
  observation of
  gonads
GI [+ or -] SD; ANOVA,             >30                      XX
  SNK test; histology
GI [+ or -] SD               [greater than                  XX
  ([dagger])([dagger])       or equal to] 60
  ([dagger])([dagger])
  ([dagger]),
  megascopic
  observation of
  oozing gonads
GI [+ or -] SD                    35-70             Increasing GI with
  ([section])                                      increasing TD at two
  ([section])                                           locations
  ([section]), *****;
  Histology
GI [+ or -] SE;                   35-70                     XX
  macroscopic smears
GI [+ or -] SE; KCI              80-110                     XX
  injection
GI [+ or -] SD; ANOVA,           41-100                     XX
  Tukey's test;
  histology
GI [+ or -] SD;                Mean sizes                   XX
  histology                   ranged from
                                  46-59
GI (as boxplot);                  65-85                     XX
  Kruskal-Wallis,
  Dunn's tests
GI [+ or -] SE                    30-60                     XX
  ([section])
  ([section])
  ([section])
  ([section]); ANOVA,
  Tukey's test,
  histology
GI [+ or -] SD                     >33                      XX
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
   Kruskal-Wallis
   test; histology
GI [+ or -] SE;                    >23                      XX
  Kruskal-Wallis,
  Tukey's tests
GI [+ or -] SD                    45-55                     XX
  ([parallel])
  ([parallel])
  ([parallel])
GI [+ or -] SE;                    >16                      XX
  Kruskal-Wallis,
  Dunn's tests;
  histology
GI [+ or -] SD                     >40                      XX
  ([section])
  ([section])
  ([section])
  ([section])
  ([section]); paired
  sample tests; KC1
  injection
GI [+ or -] 95% CI;               30-43                     XX
  histology                   ([paragraph])
                              ([paragraph])
                              ([paragraph])
                              ([paragraph])
                              ([paragraph])
                                  55-70
                              ([parallel])
                              ([parallel])
                              ([parallel])
                              ([parallel])
                              ([parallel])
GI ([Q.sub.2] with 5th            65-85                     XX
  and 95lh)
   percentiles;
  Kruskal-Wallis,
  Dunn's tests;
  histology
GI [+ or -] 95% CI;              60-102                     XX
   Kruskal-Wallis,
  Dunn's tests;
  histology
GI ******                        <10-65                     X
                               ([dagger])
                               ([dagger])
                               ([dagger])
                               ([dagger])
                               ([dagger])
                               ([dagger])
GI [+ or -] SE ***;                >21                      X
  ANOVA; KC1
  injection; histology
GI [+ or -] SE;                 28.1-44.9                   XX
  Kruskal-Wallis,
  Steel-Dwass tests;
  histology
GI [+ or -] SD; ANOVA,             nd                       XX
  Tukey's multiple
  comparisons
Mean gonadal weight             25-130 g                    X
  [+ or -] 95% CI              (median wet
                                 weight)
SGI ([double dagger])             >40.5                     XX
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
  nonlinear mixed
  regression model
GI [+ or -] SE                 62.9-121.0                   XX
  ([paragraph])
  ([paragraph]);
  ANOVA, Tukey's HSD
  test; histology;
  oocyte size-
  frequency
  distribution
GI [+ or -] SE;                 35.0-58.6                   X
  Kruskal-Wallis,
  Dunn's tests;
  histology

How spawning
was assessed                    Species                 Location

Direct observation       Diadema setosum         Suez, Egypt
Extrusion of ripe        Psammechinus miliaris   Keppel, Millport,
  ova; appearance of     Echinus esculentus        Scotland, Clyde
  larvae and early                                 Sea
  juveniles
Fertilization trials     E. esculentus           Plymouth, United
                                                   Kingdom
Observation of spent     E. esculentus           Port Erin, Isle of
  individuals                                      Man, Irish Sea
  ([dagger])
  microscopy
GI ([double dagger]);    E. esculentus           Port Erin, Isle of
  microscopy                                       Man, Irish Sea
Direct observation of    Echinocardium           Port Erin, Isle of
  gonad releasing          cordatum                Man, Irish Sea
  gametes;
  microscopy;
  histology
Sperm agglutination      Strongylocen trotus     Droback, Trondheim,
  tests both species       droebachiensis          Tromso, Norway
                           Strongylocentrotus
                           pallidus
GI ([section])           Strongylocentrotus      Pescadero Point, CA
                           purpuratus              Yankee Point, CA
GI [+ or -] 95% CI       Mesocentrotus           Pescadero Point, CA
  ([section])              franciscanus
GI [+ or -] 95% CI       S. purpuratus           Hopkins Marine Station
  ([section])
Visual assessment of     S. droebachiensis       Salisbury Cove, ME
  gonad ripeness
GI distribution plots    S. purpuratus           Yankee Point, CA
  ([section])                                      Moss Beach, CA
GI ([paragraph]);        Tripneustes             Barbados, West Indies
  plankton tows for        ventricosus
  larvae
GI ([section])           S. purpuratus           Baja California
                                                   Coos Head, OR
GI ([section]);          Strongylocentrltus      Monterey Bay, CA
  fertilization            fragilis
  studies
GI [+ or -] 95% CI       S. purpuratus           Yankee Point, CA
  ([section])                                      Pescadero Point, CA
GI [+ or -] SE           Mesocentrotus nudus     Muroran, Ishiya, and
  ([parallel]);            Strongylocentrotus      Shinori southern
  histology for both       intermedius             Hokkaido, Japan
  species
GI ([double dagger])     Lytechinus variegatus   Virginia Key, Miami,
                                                   FL Richardson's
                                                   Cove Bermuda
GI ([double dagger])     T. ventricosus          Virginia Key, Miami,
                                                   FL
GI [+ or -] SD           Stomopneustes           Madras Harbor, India
  ([section])              variolaris
Direct observation       Diadema antillarum      St. John, U.S.
                                                   Virgin Islands
GI [+ or -] SD           S. purpuratus           Yankee Point, CA
GI ([double dagger]);    T. ventricosus          Virginia Key, FL
  microscopy
GI ([section])           S. purpuratus           Pacific Grove, CA
GI [+ or -] 95% CI       Ar bacia punctulata     Woods Hole, MA
  ([section])
GI ([paragraph];         D. anliUarum            St. James, Barbados,
  microscopy                                       West Indies
GI [+ or -] SE           S. droebachiensis       Lamoine. ME
  ([section])
GI [+ or -] SE           S. intermedins          Volcano Bay, Tugaru
  ([parallel]);                                    Straits, and Japan
  microscopy                                       Sea, southern
                                                   Hokkaido, Japan
Histology                Stvlocidaris affinis    Between Isle of Capri
                                                   and Bocca Piccola,
                                                   Italy
GI ([double dagger]);    D. setosum              Seto (Aichi
  microscopy; KC1                                  Prefecture), Japan
  injection
GI [+ or -] 95% CI       Arbacia lixula          Villenfranche, France
  ([section]);           Paracentrotus lividus
  histology ; %          Psammechinus
  mature                   microtuberculatus
GI [+ or -] 95% CI       Eucidaris tribuloides   Margot Fish Shoal,
  ([double dagger]);                               Virginia Key, Long
  microscopy;                                      Reef, South
  histology                                        Florida, FL
Direct observation;      D. setosum              Indo-Pacific region
  histology              Echinometra mathaei
Histology                E. mathaei              Rottnest Island,
                                                   Western Australia
Histology                P. microtuberculatus    Gulf of Naples, Italy
GI [+ or -] error        Tripneustes gratilla    Seto (Aichi
  bars ([double          E. mathaei                Prefecture),
  dagger]);              Heliocidaris              Shirahama (Wakayama
  microscopy               crassispina
                         Echinostrephus            Prefecture), Japan
                           aciculatus
GI ([double dagger]);    Echinometra lucunter    Virginia Key to Pigeon
  microscopy;            Echinometra viridis       Key, South Florida,
  histology                                        FL
GI [+ or -] SD;          Prionocidaris           Wadi el Dome,
  ANOVA; direct            baculosa                northwestern
  observation;           Lovenia elongata          Gulf of Suez
  histology
GI [+ or -] SD;          E. mathaei              Gulf of Suez,
  direct observation;                              northwestern
  histology                                        Red Sea, Egypt
GI ([double dagger]);    Evechinus               Kaiteriteri, South
  microscopy               chloroticus             Island Kaikoura,
                                                   South Island New
                                                   Zealand
GI [+ or -] SD;          D. setosum              Gulf of Suez and
  histology                                        northern Red Sea
GI ([double dagger])     L. variegatus           Bear Cut Flats and
                                                   Sewage Beach, Miami,
                                                   FL
Microscopy; histology    Centrostephanus         Santa Catalina Island,
  ([dagger])               coronatus               CA
  ([dagger])
GI; microscopy           S. droebachiensis       Cape Cod Bay, MA
  (proportion of ripe    S. droebachiensis         Boothbay Harbor, ME
  eggs from the
  population)
Histology                S. purpuratus           Central Oregon
GI[+ or -] 95% CI        S. purpuratus           Central Oregon
  ([double dagger])
  ([double dagger]);
  histology
Direct observation       S. droebachiensis       St. Margaret's Bay,
                                                   Nova Scotia
Percent of urchins       S. purpuratus           Paios Verdes, CA
  oozing gametes
GI [+ or -] 95% CI       P. lividus              Bantry Bay, Ireland
  ([section])
  ([section])
Direct observation;      S. droebachiensis       Burrard Inlet,
  GI [+ or -] 95% CI                               Vancouver, British
                                                   Columbia
Percent of urchins       C. coronatus            Santa Catalina
  oozing gametes;                                  Island, CA
  oocyte size-
  frequency
  distribution;
  histology
GI([double dagger]);     D. antillarum           Indian Key and Key
  histology                                        West, FL
GI [+ or -] error        M. franciscanus         Amphitrite Point,
  bars (undefined)                                 Vancouver Island,
  ([paragraph])                                    British Columbia
  ([paragraph]);
  histology
GI [+ or -] SE;          Heliocidaris            Derwent Estuary,
  microscopy;              erythrogramma           Blubber Heads,
  histology                                        southeastern
                                                   Tasmania
GI [+ or -] error        H. crassispina          Mouth of Tokyo Bay,
  bars (undefined);      Hemicentrotus             Japan
  microscopy;              pulcherrimus
  histology
GI ([paragraph])         S. droebachiensis       San Juan Islands, WA
  ([paragraph])
GI ([parallel])          Loxechinus albus        Valparaiso, Chile
  ([parallel]);
  histology
GI [+ or -] 95% CI;      S. droebachiensis       Portugal Cove,
  ANOVA (undefined a     S. droebachiensis         Newfoundland First
  posteriori test)       S. purpuratus             Narrows & Botanical
                                                   Beach, Vancouver
                                                   Island, British
                                                   Columbia
GI [+ or -]2 SE          Centrostephanus         Solitary Islands, New
  ([double dagger]);       rodgersii               South Wales,
  histology (for each    Phyllacanthus             Australia
  species)                 parvispinus
                         Heliocidaris
                           tuberculata
                         T. gratilla
GI for both species;     T. gratilla             Puerto Galera, Mindoro
  histology for T.       D. setosum                Island, Philippines
  gratilla
GI                       Parechinus angulosus    Robben Island; Oatland
                                                   Point, near
                                                   Capetown, South
                                                   Africa
Histology for each       Asthenosoma ijimai      Kanagawa, Japan
  species                Araeosoma owstoni
                         H. pu/cherrimus
                         H. crassispina
                         Pseudocentrotus
                           depressus
GI [+ or -] SE;          T. gratilla             Kuei-hou and Yeh-liu,
  histology                                        northern Taiwan
GI [+ or -] SD           L. variegatus           Anclote Estuary, FL
  ([double dagger])
  ([double dagger]);
  histology
Adjusted mean GI         Diadema mexicanum       Island of Uraba,
  [+ or -] 95%           Echinometra vanbrunti     Panama Culebra
  CI ***; microscopy     D. antillarum             Island, Panama Maria
  for all species        E. viridis                Chiquta, Panama Fort
                         E. lucunter               Randolph, Panama
GI [+ or -] SD           D. antillarum           Castle Harbour,
  ([double dagger]);                               Bermuda
  histology; oocyte
  size-frequency
  distribution
Changes in adjusted      E. chloroticus          Hauraki Gulf, New
  GV through time;                                 Zealand
  histology
GI [+ or -] SD;          S. droebachiensis       Troms0ysundet, Norway
  seawater-induced       S. pallidas
  gamete release;
  histology for both
  species
GI [+ or -]SE            S. droebachiensis       Conception Bay,
                                                   Newfoundland
GI ([double dagger]);    E. lucunter             Little Bay, Graves
  microscopy                                       End, Barbados
Oocyte size-frequency    Gracilechinus affinis   Rockall Trough,
  distribution;                                    northeast Atlantic
  histology                                        Ocean
KC1 injection            T. ventricosus          San Bias Islands,
                         L. variegatus             Panama
                         E. viridis
                         Lytechinus williamsi
                         E. lucunter
GI [+ or -] 95% CI       E. esculentus           Plymouth and Cornwall,
  ([dagger])([dagger])                             England
  ([dagger]); oocyte
  size-frequency
  distribution;
  histology
Proportion of            S. droebachiensis       Eastern Newfoundland
  population observed                              (4 sites)
  to be spawning
Direct observation;      D. antillarum           Lameshur Bay, St. John
  KC1 injection;                                  U.S. Virgin Islands
  [bar.x] percent
  spawning [+ or -] SD
[bar.x] [+ or -] 95%     E. esculentus           Duart and Cuan,
  CI gonad dry weight                              Scottish West Coast
  through time; %
  mature gonads;
  microscopy
GI [+ or -] SD           P. lividus              Ballynahown and
  ([double dagger])                                Glinsk, western
  ([double dagger]):                               coast of Ireland
  histology
GI [+ or -] SD;          Heterocentrotus         Gulf of Aqaba, Red
  histology; KC1           mamillatus              Sea
  injection;
  microscopy
GI [+ or -] SE;          S. variolaris           Oslo Beach, South
  histology                                        Africa
GI [+ or -] SE           H. erythrogramma        Botany Bay, New South
  ([double dagger])      H. tuberculata            Wales, Australia
  ([double dagger]);
  ANOVA, SNK;
  histology
GI [+ or -] SE           S. droebachiensis       Womens Bay, Kodiak,
                                                   AK
Microscopy; histology    Stylocidaris lineata    Northern Bahamas
                                                   (deep water)
GI [+ or -] SD;          L. albus                Punta Lagunillas,
  histology                                        Chile
GI [+ or -] SD           Sphaerechinus           Glenan Archipelago,
  ([section])              granulans               Western Brittany,
  ([section])                                      France
  ([section])
GI [+ or -] 95% CI;      S. droebachiensis       St. Lawrence Estuary,
  ANOVA, Scheffe's                                 Quebec, Canada
  test; direct
  observation;
  microscopy
GI [+ or -] SD;          Tetrapygus niger        Punat Lagunillas,
  histology                                        Bhaia La Herradura
                                                   de Guayacan, Chile
GI [+ or -] 95% CI;      S. droebachensis        Avachinskaya Inlet,
  histology              Strongylocentrotus        Kamchatka, Russia
                           polyacantlius
GI [+ or -] SD           S. granularis           Glenan Archipelago,
                                                   Western Brittany,
                                                   France
GI [+ or -] SE           C. rodgersii            Sydney, New South
  ([double dagger])                                Wales, Australia
  ([double dagger]);
  ANOVA, SNK test;
  KC1 injection;
  histology
GI                       P. lividus              Galicia, Spain
GI [+ or -] SE; Mest;    Diadema savignyi        Ispingo Beach,
  histology for both     E. mathaei                Ramsgate, Natal
  species                                          Province, South
                                                   Africa
GI [+ or -] SE           P. lividus              Tossa de Mar,
  ([paragraph])                                    Cubelles, northeast
  ([paragraph])                                    coast of Spain
  ([paragraph]);
  ANOVA, Tukey's
  test; histology
GI [+ or -] SE           E. chloroticus          North and southwest
  ([section]); ANOVA,                              coast South Island,
  SNK test                                         New Zealand

GI [+ or -] 95% CI       P. lividus              Urbinu lagoon; East
  ([parallel])                                     coast of Corsica,
  ([parallel])                                     France
 ([parallel]); ANOVA,
  Tukey's HSD test
GI [+ or -] 95% CI;      H. crassispina          Mera Bay, within
  histology                                        Suruga Bay, Shizuoka
                                                   Prefecture, Japan
GI [+ or -] SE;          C. rodgersii            New South Wales,
  histology                                        Australia (4
                                                   locations)
Seasonal changes in      E. esculentus           Isle of Cumbrae, Clyde
  mean gonad dry                                   Estuary, Scotland
  weight
GI [+ or -] 95% CI       P. lividus              Urbinu lagoon; East
  ([parallel])                                     coast of Corsica,
  ([parallel])                                     France
  ([parallel])
GI [+ or -] SD           S. granulans            Bay of Brest, West
  ([section])                                      Brittany, Brittany,
  ([section])                                      France
  ([section]);
  histology
GI [+ or -] SE           E. chloroticus          Doubtful Sound, South
  ([paragraph])                                    Island, New Zealand
  ([paragraph]);
  direct observations
GI [+ or -] SE           E. chloroticus          Doubtful Sound-
  ([paragraph])                                    Thompson Sound,
  ([paragraph]);                                   South Island, New
  direct observations                              Zealand
GI [+ or -] SD;          S. droebachiensis       Mahone Bay and St.
  ANOVA; histology                                 Margaret's Bay,
                                                   Nova Scotia
GI [+ or -] 95% CI,      S. droebachiensis       Motovsky Bay, Barents
  histology                                        Sea, Russia
GI [+ or -] SD;          P. lividus              Morgat, southern
  histology                                        Brittany, France
KC1 injection; field     Sterechinus neumayeri   Borge Bay, Signy
  observations of                                  Island, Antarctica
  larvae
GI [+ or -] SD           S. granularis           Bay of Brest,
  ([section])                                      Britanny, France
  ([section])
  ([section]);
  Wilcoxon-Mann-
  Whitney test
GI [+ or -] error        L. albus                Cockburn Channel;
  bars (not defined);                              Dawson Isl.
  histology                                        Magallanes, Chile
GI [+ or -] SE           D. setosum              Kubbar Island reef,
  ([paragraph])          E. mathaei                Kuwait
  ([paragraph]);
  ANOVA, SNK test;
  histology
GI ([dagger])            L. variegatus           St. Joseph Bay, FL
  ([dagger])
  ([dagger])
  ([dagger]);
  microscopy; KC1
  injection
GI [+ or -] SE           E. chloroticus          Tory Channel,
  ([paragraph])                                    Marlbrorough Sounds,
  ([paragraph]);                                   New Zealand
  ANOVA; histology
GI [+ or -] SD           D. antillarum           Gran Canaria, Canary
  ([double dagger]),                               Islands
  ***
GI [+ or -]95% CI        P. lividus              Bay of Algiers; Bou
  ([parallel])                                     Ismail, Algeria
  ([parallel])
  ([parallel]);
  Kruskal- Wallis,
  SNK tests
GI [+ or -] 95% CI       P. miliaris             Loch Creran, West
  ([double dagger])                                Scotland
  ([double dagger])
  ([double dagger])
  ([double dagger]);
  histology
GI ([parallel]);         S. intermedius          Cape Zolotoi
  histology                                        Cape Povorotnyi,
                                                   Primor'e Far
                                                   Eastern Russia
GI [+ or -] SE           S. polyacanthus         Shemya Island, AK
  ([double dagger])
  ([double dagger])
GI [+ or -] SE           E. chloroticus          Doubtful Sound, New
  ([paragraph])                                    Zealand
  ([paragraph]);
  ANOVA; histology
GI [+ or -] SD;          L. variegatus           Biscayne Bay, FL
  histology
GI [+ or -] SE           Holopneustes            Bare Island, Botany
  ([section])              purpuraseens            Bay, Australia
  ([section])
  ([section])
  ([section]); ANOVA,
  Tukey's test; KC1
  injection; histology
GI [+ or -] 95% CI       P. lividus              Cabo Raso, Portugal
GI [+ or -] SD           A. punctulata           Tampa, FL, nearshore
                         L. variegatus             and offshore
GI ****; Kruskal-        P. lividus              Corsica, France
  Wallis; histology
GI [+ or -] SD; ANOVA,   P. lividus              Strait of Gibraltar,
  Tukey's test;                                    Spain
  histology
GI [+ or -] SD; ANOVA,   P. lividus              Lorbe, Galicia,
  Tukey's B test                                   Northwestern Spain
GI [+ or -] SE; KC1      D. savignyi             Kanamai lagoon, Kenya
  injection: histology   D. setosum
GI [+ or -] SE           E. lucunter             Arraial do Cabo,
  ([paragraph])                                    Abrolhos
  ([paragraph]),                                   Archipelago, Brazil
  *****; histology
GI [+ or -] SD           H. pulcherrimus         Oshoro Bay, Hokkaido,
                                                   Japan
GI [+ or -] SD;          Pseudechinus            Puerto Madryn,
  histology                magellanicus            Argentina
GI [+ or -] SE; ANOVA,   P. lividus              Near Strait of
  Tukey's test:                                    Gibraltar (4 sites);
  histology                                        Western
                                                   Mediterranean
                                                   (2 sites)
GI [+ or -] SD *****;    H. crassispina          Kodomari, Wakasa Bay,
  histology                                        Central Japan Sea
GI [+ or -] SE           P. lividus              Atlantic coast of
  ([parallel])                                     Casablanca, Morocco
  ([parallel])
  ([parallel]); ANOVA,
  Tukey's HSD test
GI [+ or -] SD           D. savignyi             Viti Levu, Fiji
  ([section])            D. setosum
  ([section])            Echinothrix calamaris
  ([section])            Echinothrix diadema
  ([section]);
  microscopy (for each
  species)
GI [+ or -] SE: KC1      T. gratilla             Kanamai lagoon, Kenya
  injections;
  histology
GI [+ or -] SE; ANOVA;   E. mathaei              Vipingo, Kanamai,
  KC1 injections;                                  Diani lagoons,
  histology                                        Kenya
GI                       L. variegatus           Margarita Island,
                                                   Venezuela
GI [+ or -] SD; ANOVA;   T. gratilla             Beloza fringing reef
  histology                                        lagoon, southwestern
                                                   coast of Madagascar
GI [+ or -] SD; ANOVA;   H. puleherrimus         Onagawa Bay, Miyagi
  Scheffe test;                                    Prefecture, Japan
  histology
GI [+ or -] SD;          S. droebachiensis       Chedabucto Head,
  ANOVA *****                                      Halifax Harbor,
                                                   Nova  Scotia
GI [+ or -] SE; ANOVA,   S. droebachiensis       Pemaquid Point and
  Fisher's LSD, Mann                               West Boothbay
  Whitney tests                                    Harbor, ME
GI [+ or -] SE ***;      D. antillarum           Abades and Boca
  ANOVA(ns)                                        Cangrejo, Canary
                                                   Islands
GI [+ or -] SD           P. lividus              Bay of Brest
  ([section])            P. miliaris
  ([section])
  ([section]); ANOVA,
  LSD
GI [+ or -] SE;          P. magellanicus         Golfo Nuevo, Patagonia
  histology; ANOVA on                              Argentina
  mean oocyte
  diameter, Tukey's
  test
GI [+ or -] SE;          P. lividus              Ligurian coast of
  ANOVA(ns); histology                             Italy (Bergeggi, SV)
Dry gonad mass           S. neumaveri            Rothera Point,
  [+ or -] SE; KC1                                 Adelaide Island,
  injection; histology                             Antarctica
GI [+ or -] SD;          M. nudus                Coast of Tsubaki, Oga
  Kruskal-Wallis,        H. puleherrimus           Peninsula, Honshu
  Tukey's tests;                                   Prefecture, Japan
  macroscopic
  observation of
  gonads
GI [+ or -] SD; ANOVA,   S. droebachiensis       Isles of Shoals, NH
  SNK test; histology
GI [+ or -] SD           L. a/bus                Chiloe Island, Chile
  ([dagger])([dagger])
  ([dagger])([dagger])
  ([dagger]),
  megascopic
  observation of
  oozing gonads
GI [+ or -] SD           P. lividus              Bay of Tunis, Tunisia
  ([section])
  ([section])
  ([section]), *****;
  Histology
GI [+ or -] SE;          S. droebachiensis       Bodo, Norway
  macroscopic smears
GI [+ or -] SE; KCI      C. rodgersii            Eastern Tasmania
  injection
GI [+ or -] SD; ANOVA,   S. granularis           Southeast coast of
  Tukey's test;                                    Spain
  histology
GI [+ or -] SD;          S. intermedins          Hirota Bay, Iwate
  histology                                        Prefecture, Japan

GI (as boxplot);         L. albus                Bridges Island, Beagle
  Kruskal-Wallis,                                  Channel, Argentina
  Dunn's tests
GI [+ or -] SE           E. mathaei              Bostaneh, Persian
  ([section])                                      Gulf, Iran
  ([section])
  ([section])
  ([section]); ANOVA,
  Tukey's test,
  histology
GI [+ or -] SD           E. lucunter             Southern coast of
  ([double dagger])                                Pernambuco, Brazil
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
   Kruskal-Wallis
   test; histology
GI [+ or -] SE;          E. lucunter             Praia da Casta, Vila
  Kruskal-Wallis,                                  Velha, Espirito
  Tukey's tests                                    Santo, Brazil
GI [+ or -] SD           P. lividus              Algers Bay and Bay of
  ([parallel])                                     Boou-Ismail, Algeria
  ([parallel])
  ([parallel])
GI [+ or -] SE;          Arbacia dufresnii       Golfo Nuevo,
  Kruskal-Wallis,                                  Patagonia, Argentina
  Dunn's tests;
  histology
GI [+ or -] SD           P. lividus              Southeastern Bay of
  ([section])                                      Biscay
  ([section])
  ([section])
  ([section])
  ([section]); paired
  sample tests; KC1
  injection
GI [+ or -] 95% CI;      P. lividus              Cantabrian Sea, Bay of
  histology                                        Biscay, France

GI ([Q.sub.2] with 5th   L. albus                Bridges Island, Beagle
  and 95lh)                                        Channel, Argentina
   percentiles;
  Kruskal-Wallis,
  Dunn's tests;
  histology
GI [+ or -] 95% CI;      L. albus                Port William and
   Kruskal-Wallis,                                 Berkeley Sound,
  Dunn's tests;                                    Falkland Islands
  histology
GI ******                P. lividus              Bistrina Bay, Adriatic
                                                   Sea, Croatia
GI [+ or -] SE ***;      D. ant ill arum         Tenerife Island,
  ANOVA; KC1                                       Canary Islands
  injection; histology
GI [+ or -] SE;          H. pulcherrimus         Matsushima Bay, Miyagi
  Kruskal-Wallis,                                  Prefecture, Japan
  Steel-Dwass tests;
  histology
GI [+ or -] SD; ANOVA,   P. lividus              Gulf of Tunis, Tunisia
  Tukey's multiple
  comparisons
Mean gonadal weight      S. purpuratus           Seppings Island,
  [+ or -] 95% CI                                  British Columbia to
                                                   Punta Baja, Baja
                                                   California
SGI ([double dagger])    P. lividus              Galacia coast (NW
  ([double dagger])                                Spain)
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
  nonlinear mixed
  regression model
GI [+ or -] SE           C. rodgersii            Mokohinau Islands,
  ([paragraph])                                    Northeast New
  ([paragraph]);                                   Zealand
  ANOVA, Tukey's HSD
  test; histology;
  oocyte size-
  frequency
  distribution
GI [+ or -] SE;          A. lixula               Tossa de Mar, NE Spain
  Kruskal-Wallis,
  Dunn's tests;
  histology

How spawning
was assessed                     Reference

Direct observation       Fox 1922
Extrusion of ripe        Elmhirst 1923
  ova; appearance of
  larvae and early
  juveniles
Fertilization trials     Orton 1929
Observation of spent     Stott 1931
  individuals
  ([dagger])
  microscopy
GI ([double dagger]);    Moore 1934
  microscopy
Direct observation of    Moore 1936
  gonad releasing
  gametes;
  microscopy;
  histology
Sperm agglutination      Vasseur 1952
  tests both species
GI ([section])           Lasker and Giese 1954
GI [+ or -] 95% CI       Bennett and Giese 1955
  ([section])
GI [+ or -] 95% CI
  ([section])
Visual assessment of     Harvey 1956
  gonad ripeness
GI distribution plots    Giese et al. 1958
  ([section])
GI ([paragraph]);        Lewis 1958
  plankton tows for
  larvae
GI ([section])           Boolootian and Giese 1959
GI ([section]);          Boolootian et al. 1959
  fertilization
  studies
GI [+ or -] 95% CI       Giese 1959
  ([section])
GI [+ or -] SE           Fuji 1960a
  ([parallel]);
  histology for both
  species
GI ([double dagger])     Moore et al. 1963a
GI ([double dagger])     Moore et al. 1963b
GI [+ or -] SD           Giese et al. 1964
  ([section])
Direct observation       Randall et al. 1964
GI [+ or -] SD           Lawrence et al. 1965
GI ([double dagger]);    McPherson 1965
  microscopy
GI ([section])           Boolootian 1966
GI [+ or -] 95% CI
  ([section])
GI ([paragraph];         Lewis 1966
  microscopy
GI [+ or -] SE           Cocanour and Allen 1967
  ([section])
GI [+ or -] SE           Fuji 1967
  ([parallel]);
  microscopy
Histology                Holland 1967
GI ([double dagger]);    Kobayashi and Nakamura
  microscopy; KC1          1967
  injection
GI [+ or -] 95% CI       Fenaux 1968
  ([section]);
  histology ; %
  mature
GI [+ or -] 95% CI       McPherson 1968
  ([double dagger]);
  microscopy;
  histology
Direct observation;      Pearse 1968
  histology
Histology                Pearse and Phillips 1968
Histology                Holland and Holland 1969
GI [+ or -] error        Kobayashi 1969
  bars ([double
  dagger]);
  microscopy
GI ([double dagger]);    McPherson 1969
  microscopy;
  histology
GI [+ or -] SD;          Pearse 1969a
  ANOVA; direct
  observation;
  histology
GI [+ or -] SD;          Pearse 1969b
  direct observation;
  histology
GI ([double dagger]);    Dix 1970
  microscopy
GI [+ or -] SD;          Pearse 1970
  histology
GI ([double dagger])     Moore and Lopez 1972
Microscopy; histology    Pearse 1972
  ([dagger])
  ([dagger])
GI; microscopy           Stephens 1972
  (proportion of ripe
  eggs from the
  population)
Histology                Gonor 1973a
GI[+ or -] 95% CI        Gonor 1973b
  ([double dagger])
  ([double dagger]);
  histology
Direct observation       Miller and Mann 1973
Percent of urchins       Cochran and Engelmann 1975
  oozing gametes
GI [+ or -] 95% CI       Crapp and Willis 1975
  ([section])
  ([section])
Direct observation;      Himmelman 1975
  GI [+ or -] 95% CI
Percent of urchins       Kennedy and Pearse 1975
  oozing gametes;
  oocyte size-
  frequency
  distribution;
  histology
GI([double dagger]);     Bauer 1976
  histology
GI [+ or -] error        Bernard 1977
  bars (undefined)
  ([paragraph])
  ([paragraph]);
  histology
GI [+ or -] SE;          Dix 1977
  microscopy;
  histology
GI [+ or -] error        Masuda and Dan 1977
  bars (undefined);
  microscopy;
  histology
GI ([paragraph])         Vadas 1977
  ([paragraph])
GI ([parallel])          Buckle et al. 1978
  ([parallel]);
  histology
GI [+ or -] 95% CI;      Himmelman 1978
  ANOVA (undefined a
  posteriori test)
GI [+ or -]2 SE          O'Connor et al. 1978
  ([double dagger]);
  histology (for each
  species)
GI for both species;     Tuason and Gomez 1979
  histology for T.
  gratilla
GI                       Greenwood 1980
Histology for each       Mori et al. 1980
  species
GI [+ or -] SE;          Chang-Po and Kun-Hsiung
  histology                1981
GI [+ or -] SD           Ernest and Blake 1981
  ([double dagger])
  ([double dagger]);
  histology
Adjusted mean GI         Lessios 1981
  [+ or -] 95%
  CI ***; microscopy
  for all species
GI [+ or -] SD           Iliffe and Pearse 1982
  ([double dagger]);
  histology; oocyte
  size-frequency
  distribution
Changes in adjusted      Walker 1982
  GV through time;
  histology
GI [+ or -] SD;          Falk-Petersen and Lonning
  seawater-induced         1983
  gamete release;
  histology for both
  species
GI [+ or -]SE            Keats et al. 1984b
GI ([double dagger]);    Lewis and Storey 1984
  microscopy
Oocyte size-frequency    Tyler and Gage 1984
  distribution;
  histology
KC1 injection            Lessios 1985
GI [+ or -] 95% CI       Nichols et al. 1985
  ([dagger])([dagger])
  ([dagger]); oocyte
  size-frequency
  distribution;
  histology
Proportion of            Keats et al. 1987
  population observed
  to be spawning
Direct observation;      Levitan 1988b
  KC1 injection;
  [bar.x] percent
  spawning [+ or -] SD
[bar.x] [+ or -] 95%     Comely and Ansell 1989
  CI gonad dry weight
  through time; %
  mature gonads;
  microscopy
GI [+ or -] SD           Byrne 1990
  ([double dagger])
  ([double dagger]):
  histology
GI [+ or -] SD;          Dotan 1990
  histology; KC1
  injection;
  microscopy
GI [+ or -] SE;          Drummond 1991
  histology
GI [+ or -] SE           Laegdsgaard et al. 1991
  ([double dagger])
  ([double dagger]);
  ANOVA, SNK;
  histology
GI [+ or -] SE           Munk 1992
Microscopy; histology    Young et al. 1992
GI [+ or -] SD;          Zamora and Stotz 1992
  histology
GI [+ or -] SD           Guillou and Michel 1993
  ([section])
  ([section])
  ([section])
GI [+ or -] 95% CI;      Starr et al. 1993
  ANOVA, Scheffe's
  test; direct
  observation;
  microscopy
GI [+ or -] SD;          Zamora and Stotz 1993
  histology
GI [+ or -] 95% CI;      Arkhipova and Yakovlev
  histology                1994
GI [+ or -] SD           Guillou and Michel 1994
GI [+ or -] SE           King et al. 1994
  ([double dagger])
  ([double dagger]);
  ANOVA, SNK test;
  KC1 injection;
  histology
GI                       Catoira 1995
GI [+ or -] SE; Mest;    Drummond 1995
  histology for both
  species
GI [+ or -] SE           Lozano et al. 1995
  ([paragraph])
  ([paragraph])
  ([paragraph]);
  ANOVA, Tukey's
  test; histology
GI [+ or -] SE           McShane et al. 1996
  ([section]); ANOVA,
  SNK test
GI [+ or -] 95% CI       Fernandez and Boudouresque
  ([parallel])             1997
  ([parallel])
 ([parallel]); ANOVA,
  Tukey's HSD test
GI [+ or -] 95% CI;      Horii 1997
  histology
GI [+ or -] SE;          Byrne et al. 1998
  histology
Seasonal changes in      Emson and Moore 1998
  mean gonad dry
  weight
GI [+ or -] 95% CI       Fernandez 1998
  ([parallel])
  ([parallel])
  ([parallel])
GI [+ or -] SD           Guillou and Lumingas 1998
  ([section])
  ([section])
  ([section]);
  histology
GI [+ or -] SE           Lamare 1998
  ([paragraph])
  ([paragraph]);
  direct observations

GI [+ or -] SE           Lamare and Stewart 1998
  ([paragraph])
  ([paragraph]);
  direct observations
GI [+ or -] SD;          Meidel and Scheibling 1998
  ANOVA; histology
GI [+ or -] 95% CI,      Oganesyan 1998
  histology
GI [+ or -] SD;          Spirlet et al. 1998
  histology
KC1 injection; field     Stanwell-Smith and Peck
  observations of          1998
  larvae
GI [+ or -] SD           Guillou and Lumingas 1999
  ([section])
  ([section])
  ([section]);
  Wilcoxon-Mann-
  Whitney test
GI [+ or -] error        Oyarzun et al. 1999
  bars (not defined);
  histology
GI [+ or -] SE           Alsaffar and Lone 2000
  ([paragraph])
  ([paragraph]);
  ANOVA, SNK test;
  histology
GI ([dagger])            Beddingfield and
  ([dagger])               McClintock 2000
  ([dagger])
  ([dagger]);
  microscopy; KC1
  injection
GI [+ or -] SE           Brewin et al. 2000
  ([paragraph])
  ([paragraph]);
  ANOVA; histology
GI [+ or -] SD           Garrido et al. 2000
  ([double dagger]),
  ***
GI [+ or -]95% CI        Guettaf et al. 2000
  ([parallel])
  ([parallel])
  ([parallel]);
  Kruskal- Wallis,
  SNK tests
GI [+ or -] 95% CI       Kelly 2000
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
  histology
GI ([parallel]);         Viktorovskaya and Matveev
  histology              2000
GI [+ or -] SE           Konar 2001
  ([double dagger])
  ([double dagger])
GI [+ or -] SE           Lamare et al. 2002
  ([paragraph])
  ([paragraph]);
  ANOVA; histology
GI [+ or -] SD;          McCarthy and Young 2002
  histology
GI [+ or -] SE           Williamson and Steinberg
  ([section])              2002
  ([section])
  ([section])
  ([section]); ANOVA,
  Tukey's test; KC1
  injection; histology
GI [+ or -] 95% CI       Gago et al. 2003
GI [+ or -] SD           Hill and Lawrence 2003
GI ****; Kruskal-        Leoni et al. 2003
  Wallis; histology
GI [+ or -] SD; ANOVA,   Martinez et al. 2003
  Tukey's test;
  histology
GI [+ or -] SD; ANOVA,   Montero-Torreiro and
  Tukey's B test           Garcia-Martinez 2003
GI [+ or -] SE; KC1      Muthiga 2003
  injection: histology
GI [+ or -] SE           Ventura et al. 2003
  ([paragraph])
  ([paragraph]),
  *****; histology
GI [+ or -] SD           Agatsuma and Nakata 2004
GI [+ or -] SD;          Bigatti et al. 2004
  histology
GI [+ or -] SE; ANOVA,   Sanchez-Espana et al. 2004
  Tukey's test:
  histology
GI [+ or -] SD *****;    Yatsuya and Nakahara 2004
  histology
GI [+ or -] SE           Bayed et al. 2005
  ([parallel])
  ([parallel])
  ([parallel]); ANOVA,
  Tukey's HSD test
GI [+ or -] SD           Coppard and Campbell 2005
  ([section])
  ([section])
  ([section])
  ([section]);
  microscopy (for each
  species)
GI [+ or -] SE: KC1      Muthiga 2005
  injections;
  histology
GI [+ or -] SE; ANOVA;   Muthiga and Jaccarini 2005
  KC1 injections;
  histology
GI                       Quijano and Gaspar 2005
GI [+ or -] SD; ANOVA;   Vaitilingon et al. 2005
  histology
GI [+ or -] SD; ANOVA;   Agatsuma et al. 2006
  Scheffe test;
  histology
GI [+ or -] SD;          Brady and Scheibling 2006
  ANOVA *****
GI [+ or -] SE; ANOVA,   Gaudette et al. 2006
  Fisher's LSD, Mann
  Whitney tests
GI [+ or -] SE ***;      Hernandez et al. 2006
  ANOVA(ns)
GI [+ or -] SD           Jacquin et al. 2006
  ([section])
  ([section])
  ([section]); ANOVA,
  LSD
GI [+ or -] SE;          Marzinelli et al. 2006
  histology; ANOVA on
  mean oocyte
  diameter, Tukey's
  test
GI [+ or -] SE;          Barbaglio et al. 2007
  ANOVA(ns); histology
Dry gonad mass           Brockington et al. 2007
  [+ or -] SE; KC1
  injection; histology
GI [+ or -] SD;          Endo et al. 2007
  Kruskal-Wallis,
  Tukey's tests;
  macroscopic
  observation of
  gonads
GI [+ or -] SD; ANOVA,   Harrington et al. 2007
  SNK test; histology
GI [+ or -] SD           Kino and Agatsuma 2007
  ([dagger])([dagger])
  ([dagger])([dagger])
  ([dagger]),
  megascopic
  observation of
  oozing gonads
GI [+ or -] SD           Sellem and Guillou 2007
  ([section])
  ([section])
  ([section]), *****;
  Histology
GI [+ or -] SE;          Hagen et al. 2008
  macroscopic smears
GI [+ or -] SE; KCI      Ling et al. 2008
  injection
GI [+ or -] SD; ANOVA,   Martinez-Pita et al. 2008
  Tukey's test;
  histology
GI [+ or -] SD;          Matsui et al. 2008
  histology
GI (as boxplot);         Perez et al. 2008
  Kruskal-Wallis,
  Dunn's tests
GI [+ or -] SE           Shahri et al. 2008
  ([section])
  ([section])
  ([section])
  ([section]); ANOVA,
  Tukey's test,
  histology
GI [+ or -] SD           Lima et al. 2009
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
   Kruskal-Wallis
   test; histology
GI [+ or -] SE;          Mariante et al. 2009
  Kruskal-Wallis,
  Tukey's tests
GI [+ or -] SD           Soualili and Guillou 2009
  ([parallel])
  ([parallel])
  ([parallel])
GI [+ or -] SE;          Brogger et al. 2010
  Kruskal-Wallis,
  Dunn's tests;
  histology
GI [+ or -] SD           Garmendia et al. 2010
  ([section])
  ([section])
  ([section])
  ([section])
  ([section]); paired
  sample tests; KC1
  injection
GI [+ or -] 95% CI;      Gonzalez-Irusta et
  histology                al. 2010
GI ([Q.sub.2] with 5th   Perez et al. 2010
  and 95lh)
   percentiles;
  Kruskal-Wallis,
  Dunn's tests;
  histology
GI [+ or -] 95% CI;      Schuhbauer et al. 2010
   Kruskal-Wallis,
  Dunn's tests;
  histology
GI ******                Tomsic et al. 2010
GI [+ or -] SE ***;      Hernandez et al. 2011
  ANOVA; KC1
  injection; histology
GI [+ or -] SE;          Ogasawara et al. 2011
  Kruskal-Wallis,
  Steel-Dwass tests;
  histology
GI [+ or -] SD; ANOVA,   Arafa et al. 2012
  Tukey's multiple
  comparisons
Mean gonadal weight      Ebert et al. 2012
  [+ or -] 95% CI
SGI ([double dagger])    Ourens et al. 2013
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger])
  ([double dagger]);
  nonlinear mixed
  regression model
GI [+ or -] SE           Pecorino et al. 2013
  ([paragraph])
  ([paragraph]);
  ANOVA, Tukey's HSD
  test; histology;
  oocyte size-
  frequency
  distribution
GI [+ or -] SE;          Wangensteen et al. 2013
  Kruskal-Wallis,
  Dunn's tests;
  histology

LSD, least significant difference; nd, no data given; x, no
analyses performed; xx, indicated knowledge about size/gonad
relationship (sensu Fuji 1960b; Moore et al. 1963a; Pearse 1970;
Gonor 1972); xo, size of the urchins was restricted to a specific
range, but no indication of a size/gonadal relationship was given.

Direct observation refers to visual examination of the gonads
either in the field and/or the laboratory.

ANOVA indicates an overall (global) significant (P [less than or
equal to] 0.05) F-test for temporal variability without an a
posteriori test; ANOVA(ns) indicates an overall (global)
nonsignificant (P > 0.05) F-test for temporal variability.

ANOVA, SNK, or some other a posteriori or a priori test indicates
an overall F-test for temporal variability and a subsequent
comparison of means to pinpoint when spawning occurred.

In some cases, higher stats may have been used, but not as a test
to determine when spawning occurred.

* GI = wet weight of gonad divided by total wet weight of animal X
100 (unless otherwise noted). TD = Test diameter,

([dagger]) Chemical and graphical determinations on gonad-specific
gravity, dry weights, and glycogen levels,

([double dagger]) GI = (10 X GV) divided by test volume. GV = gonad
volume.

([section]) GI = GV divided by total wet weight of urchin.

([paragraph]) GI = GV divided by TD (for Lewis 1966, GI = GV
divided by TD cubed)

([parallel]) GI = gonad wet weight divided by total volume of
urchin.

** Showed a positive relationship between GV and TD between 20 and
30 mm; no trend after 30 mm TD.

([dagger])([dagger]) Spawning assessed using gross observations
(size of gonads), change in thickness of spermatocytes,
spermatozoa, oocyte diameter, and nutritive phagocytes.

([double dagger])([double dagger]) GI = gonad dry weight divided by
total dry weight.

([section])([section]) GI = gonad wet weight divided by total wet
weight minus the gonad wet weight.

([paragraph])([paragraph]) GI = gonad wet weight divided by drained
test weight.

([parallel])([parallel]) GI = gonad wet weight divided by TD cubed
(i.e., TD3).

*** GI = GV divided by dry body weight

([dagger])([dagger])([dagger]) GI = eviscerated dry weight (g)
divided by total body volume (ml).

([double dagger])([double dagger])([double dagger]) Gamete volume
increased allometrically with TD.

([section])([section])([section]) GI = gonad dry weight divided by
eviscerated test dry weight.

([paragraph])([paragraph])([paragraph]) GI = gonad dry weight (of
four lobes) divided by dry body weight (we assume "body weight" and
total weight are the same).

([parallel])([parallel])([parallel]) GI = gonad dry weight divided
by TD cubed (expressed either in cm3 or mm3).

**** "Gonad retrieval rate, GRR" = slope of a regression of gonad
weight against total weight; GRR used instead of GI; ANOVA used to
determine location and habitat effects on GRR, but not used to
determine when spawning occurred.

([dagger])([dagger])([dagger])([dagger]) Data were purportedly
analyzed statistically, but no P values, error bars, etc. are
provided. ([double dagger])([double dagger])([double
dagger])([double dagger]) GI = gonad wet weight divided by the wet
weight of the eviscerated test expressed as a percentage.

([section])([section])([section])([section]) GI = gonad dry weight
(of four lobes, corrected to five lobes) divided by total dry
weight.

([paragraph])([paragraph])([paragraph])([paragraph]) Ranges were
estimated from Table 3 in Hill and Lawrence (2003).

([parallel])([parallel])([parallel])([parallel]) Standard error
(Table 1 in Muthiga 2003)

***** ANOVA or Mann-Whitney U-test was used to determine difference
in mean GI between sites, years, or depths, but not used to assess
spawning

([dagger])([dagger])([dagger])([dagger])([dagger]) Error bars
given, and it is assumed that they represent 1 SD (Table 1 in Kino
& Agatsuma 2007)

([double dagger])([double dagger])([double dagger])([double
dagger])([double dagger]) GI = [dry weight of 4 gonads/dry weight
of dissected test - (gonads + gut contents)] X 100.

([section])([section])([section])([section])([section]) GI was
calculated using four methods (three are listed here as footnotes
*, ([double dagger]) ([double dagger]),
([parallel])([parallel])([parallel]), and dry gonad weight divided
by whole animal wet weight.

([paragraph])([paragraph])([paragraph])([paragraph])([paragraph])
Intertidal collection.

([parallel])([parallel])([parallel])([parallel])([parallel])
Subtidal collection.

****** GI given with some estimate of error that was undefined.
([dagger])([dagger])([dagger])([dagger])([dagger])([dagger]) Ranges
were estimated from Figures 2 and 3 in Tomsic et al. (2010).

([double dagger])([double dagger])([double dagger])([double
dagger])([double dagger])([double dagger]) Standardized GI defined
in Ourens et al. 2012.

TABLE 8.
Comparison of various formulas used to calculate GI in sea urchins.

            Gonad indices of Strongylocentrotus droebachiensis
                     calculated using formulae from:

                          Moore et     Lasker and
Site   n       GI *       al. 1963     Giese 1954   Lewis 1958

BBH    11   17.4 (4.1)   0.63 (0.16)   17.2 (4.2)   0.27 (0.07)
OWH    14   12.9 (2.1)   0.47 (0.08)   12.7 (2.0)   0.21 (0.03)
SPT    15   18.5 (3.8)   0.67 (0.14)   16.9 (3.4)   0.31 (0.06)

        Gonad indices of Strongylocentrotus
          droebachiensis calculated using
                  formulae from:

                     Crapp and    Biickle et
Site   Fuji 1960a   Willis 1975    al. 1978

BBH    6.4 (1.6)    21.7 (6.3)    0.06 (0.02)
OWH    4.7 (0.7)    14.9 (2.7)    0.05 (0.01)
SPT     7.3(1.5)    23.5 (6.2)    0.07 (0.01)

BBH. Boothbay Harbor; OWH, Owl's Head; SPT, Schoodic Point.

Values are means [+ or -] 95% CI from a site selected from each
region in this study from February 1988. (See Table 7 footnotes for
GI formulas associated with each reference.).

* (Total wet weight of gonad/total body weight) X 100; this study.
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Author:Vadas, Robert L., Sr.; Beal, Brian F.; Dudgeon, Steven R.; Wright, Wesley A.
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1USA
Date:Dec 1, 2015
Words:26965
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