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1 September 2015 Spatial and Temporal Variability of Spawning in the Green Sea Urchin Strongylocentrotus droebachiensis along the Coast of Maine
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Abstract

The timing and spatial variation in spawning in the green sea urchin Strongylocentrotus droebachiensis (Müller) 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 ≥64 mm. In the central region, the size at independencewas ≥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 °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.

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 (Lefèrve & 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 morhua) 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 (Rodríguez 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, Ouréns 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 °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×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 m2, 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.

Figure 1.

Nine study sites along the Maine coast where sea urchins were sampled approximately monthly from September 1987 to 1988.

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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) × 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) × (gonad weight), r2 = 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, Ouréns 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.

TABLE 1.

Description of nine study sites, covering a distance of 270 km, and mean density in 0.25 m2 quadrats (mean number of individuals per 1 m2 % 95% CI in May to June 1988) of Strongylocentrotus droebachiensis in three coastal regions of Maine.

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To determine ifGI varied temporally and spatially, amodel 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 °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 °C. Also, field observations were made by Harvey (1956) and Cocanour & Allen (1967) who noted that temperatures above 4 °C were associated with gamete release. For example, the first contrast (fi01_1097.gif versus fi02_1097.gif) was based on seawater temperature values <4 °C versus ≥4 °C. The second contrast (fi03_1097.gif versus fi04_1097.gif) examined if GI changed significantly during winter. The third contrast (fi05_1097.gif versus fi06_1097.gif) tested whether changes in GI occurred when seawater temperatures were immediately >4 °C. The fourth contrast (fi07_1097.gif versus fi08_1097.gif) 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 (α′ = 1 - α1/m; where α = 0.05 and m = 4) based on Winer et al. 1991; therefore α′ = 0.0127. Unplanned comparisons of mean GI between sampling dates were carried out using the Bonferroni corrected t-tests using a decision rule of α = 0.05, or the a posteriori Student-Neumann-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 preand 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 m2 to nearly 70 per m2. Individuals were aggregated at one of the three sites [Bailey Island;Morisita's Index (Id = 1.57, P = 0.002)]. Densities at central sites, Stonington and Lamoine, varied greatly (5 and 30 per m2, respectively), and were aggregated at Lamoine (Id = 1.16, P = 0.012).Among the northeastern sites, urchins at Schoodic Point were aggregated only at the deepest depth (6–8 m; Id = 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 (fi09_1097.gif = 1.3 per m2). 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 (Id = 1.87, P = 0.065).

Sea Urchin Sizes

Urchins collected at all sites averaged >60 mm TD (Fig. 2) and >30mmin height (data not shown), except Lamoine where animals consistently had the smallest test sizes [fi09_1097.gif ± 95%confidence interval (CI) = 49.7 ± 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 = axb) produced the highest coefficient of determination for these data (a = 0.004, b = 1.86, r2 = 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 (r2 = 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 ≥ 60 mm, the linear, quadratic, and allometric models yielded highly significant P values, although r2 values were low. At TD ≥62.5 mm, only the quadratic model was statistically significant (Table 2). At TD ≥ 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 ≥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 ≥64mm 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 × 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 ≥64mmsubset), we presentmeanGI data for the full range of urchin sizes from each site (Figs. 57).

Figure 2.

Sea urchin TD from nine sites representing three coastal regions of Maine. Divers were asked to collect urchins >50mmdiameter from each site; however, the average size of animals at Lamoine (barren grounds) was smaller than available elsewhere.

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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. 57). Most sites, except Five Islands and Lubec, had temperatures at or below zero for one or more months. Summer temperatures were 2–10 °C cooler (maximum 10 °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. 57). 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.

Figure 3.

Relationship between GI and urchin TD for all sites and sampling dates (n = 1594). See Table 2 for lack-of fit-analyses and allometric model results for the relationship.

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Gonad Indices

Typically maximum GI occurred in late winter or early spring at the nine sites (Figs. 57). 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. 57). 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 (fi09_1097.gif ± 95% CI = 8.3 ± 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%).

TABLE 2.

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

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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. 57). 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 ( ≥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 (fi09_1097.gif ± 95% CI = 61.1 ± 7.45%, n = 9).

Figure 4.

Mean GI (%) patterns for a selected site within each coastal region (see Table 1). Solid circles represent all data from each sampling date (complete data); open circles represent data only for urchin TD ≥ 64 mm (reduced data set). SW, southwest; C, central; NE, northeast.

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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. 57) 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 °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 ± 0.5%, n = 39) and September 1988 (10.1 ± 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.

Figure 5.

Seawater temperature (open symbols with dotted lines), salinity (solid symbols and dashed lines), and mean GI (%) patterns (solid symbols and lines) for three sites comprising the southwest coast of Maine. Gonad index data include full range of test sizes.

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Mean maximum gonad index (maxGI) 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 ± 1.5%, n = 79), and was ∼52% higher than themeanmaximum from the central region (13.3 ± 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 ± 2.3%, n = 28) than urchins from Lamoine (9.1 ± 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 (r2 = 0.442, P < 0.0001, n = 1586), but an allometric model gave a significantly better fit (a = 0.00347, b = 1.721, r2 = 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.

Figure 6.

Seawater temperature (open symbols with dotted lines), salinity (solid symbols and dashed lines), and mean GI (%) patterns (solid symbols and lines) for three sites comprising the central coast of Maine. Gonad index data include full range of test sizes.

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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].

Figure 7.

Seawater temperature (open symbols with dotted lines), salinity (solid symbols and dashed lines), and mean GI (%) patterns (solid symbols and lines) for three sites comprising the northeast coast of Maine. Gonad index data include full range of test sizes.

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Overall mean TD varied significantly as a function of urchin gender (P = 0.0006). Females were, on average, 1.7 mm larger than males (fi10_1097.gif ± 95% CI = 64.6 ± 0.72 mm, n = 505; fi11_1097.gif = 62.9 ± 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 ± 0.65%) than males (11.7 ± 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 ± 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 and 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 Ouréns 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 & Lönning 1983, Munk 1992, Meidel & Scheibling 1998, Brady & Scheibling 2006).

TABLE 3.

Mean GI (%95% CI) and mean percent loss of GI for each region and site for the month before and after spawning.

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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. 58). 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. 57). 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, Gaudette 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 et 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 ≥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 1mo 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.

TABLE 4.

Summary of single-factor ANOVA results.

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Figure 8.

Mean GI (%) patterns (black squares) for a randomly selected site within each coastal region (see Table 1). Least square, adjusted means (open diamonds) and unadjusted means (open circles) for gonad wet weight. Adjusted means based on an overall mean urchin TD for Boothbay Harbor (65.5 mm), Owl's Head (63.6 mm), and Schoodic Point (66.5 mm).

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Figure 9.

Relationship between mean GI and mean ambient seawater temperature for each of the three regions: southwest: Y = 16.8 - 1.43x + 0.077x2, r2 = 0.771, n = 9, P = 0.012; central: Y = 9.7 - 0.42x, r2 = 0.553, n = 11, P = 0.009; northeast: Y = 17.7 - 0.95 x, r2 = 0.739, n 11, P = 0.0007. (Values for the central coast do not include information from Lamoine because animals there were smaller and GI were lower than elsewhere—see Results.)

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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. 57) 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. 57), 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).

TABLE 5.

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

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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 (1963a, 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 sizeindependent estimate of GI that uses information from the larger (mature) individuals in a population (Gonor 1972, Falk-Peterson & Lönning 1983, Brewin et al. 2000, Lamare et al. 2002) that may be site-specific (Sánchez-España 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., ≥64mmTD) 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).

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.

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Figure 10.

Relationship between GI and gonad wet weight for individual green sea urchins in each region. Closed circles (n = 39, 28, and 40 for southwest, central, and northeast, respectively) represent the immediate prespawning date (see Figs. 57). Open circles (n = 39, 43, 27 for southwest, central, and northeast, respectively) represent the immediate postspawning date.

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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, Oyarzún 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 (r2 = 0.75). Similarly, Vaïtilingon et al. (2005) showed GI was negatively correlated with seawater temperature (r2 = 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). Hernández 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-Décarie 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.

TABLE 7.

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

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TABLE 8.

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

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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 refugial 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./m2. 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. 57), 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, r2 = 0.013; see Figs. 57).

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, López et al. (1998) and González-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 Echinometra mathaei coincided with a peak in phytoplankton abundance. Spawning in other echinoderms (e.g., Cucumaria frondosa, 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 (Platt 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 °C (Figs. 57), 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,Keats et al. 1987, Young et al. 1992,King et 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. Ouréns 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 1965Tripneustes ventricosus; Dix 1970Evechinus chloroticus; Gonor 1973aStrongylocentrotus 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 aGI 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, Ouréns et al. 2012, 2013).

Many of the qualitative estimates used to assess spawning that are described in Table 7 included means ± 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, Scheffé) 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 (18,800mt, worth $26.8 million); however, by 1997, landings fell below 10,000mt, 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. 67). 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, Ouréns et 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 Ouréns 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. Ouréns 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).

LITERATURE CITED

  1. Y. Agatsuma 2001a. Ecology of Strongylocentrotus intermedius. In: J.M. Lawrence , editor. Edible sea urchins: biology and ecology. New York: Elsevier. pp. 333–346. Google Scholar

  2. Y. Agatsuma 2001b. Ecology of Strongylocentrotus nudus. In: J. M. Lawrence , editor. Edible sea urchins: biology and ecology. New York: Elsevier. pp. 347–361. Google Scholar

  3. Y. Agatsuma & A. Nakata . 2004. Age determination, reproduction and growth of the sea urchin Hemicentrotus pulcherrimus in Oshoro Bay, Hokkaido, Japan. J. Mar. Biol. Assoc. U.K. 84:401–405. Google Scholar

  4. Y. Agatsuma , H. Yamada & K. Taniguchi . 2006. Distribution of the sea urchin Hemicentrotus pulcherrimus along a shallow bathymetric gradient in Onagawa Bay in northern Honshu, Japan. J. Shellfish Res. 25:1027–1036. Google Scholar

  5. A. H. Alsaffar & K. P. Lone . 2000. Reproductive cycle of Diadema setosum and Echinometra mathaei (Echinoidea: Echinodermata) from Kuwait (Northern Arabian Gulf). Bull. Mar. Sci. 67:845–856. Google Scholar

  6. S. Arafa , M. Chouaibi , S. Sadok & A. El Abed . 2012. The influence of season on the gonad index and biochemical composition of the sea urchin Paracentrotus lividus from the Golf of Tunis. Sci. World J. 2012: Article ID 815935, 8 pp. doi: 10.1100/2012/815935. Google Scholar

  7. E. A. Arkhipova & S. N. Yakovlev . 1994. Annual gonadal cycles of sea urchins Strongylocentrotus polyacanthus and S. droebachiensis in Avachinskaya Inlet, Eastern Kamchatka. Russ. J. Mar. Biol. 20:303–305. Google Scholar

  8. A. Barbaglio , M. Sugni , C. Di Benedetto , F. Bonasoro , S. Schnell , R. Lavado , C. Porte & D. M. Candia Carnevali . 2007. Gametogenesis correlated with steroid levels during the gonadal cycle of the sea urchin Paracentrotus lividus (Echinodermata: Echinoidea). Comp. Biochem. Physiol., Part A. Mol. Integr. Physiol. 147:466–474. Google Scholar

  9. J. C. Bauer 1976. Growth, aggregation, and maturation in echinoid, Diadema antillarum. Bull. Mar. Sci. 26:273–277. Google Scholar

  10. A. Bayed , F. Quiniou , A. Benrha & M. Guillou . 2005. The Paracentrotus lividus populations from the northern Moroccan Atlantic coast: growth, reproduction and health condition. J. Mar. Biol. Assoc. U.K. 85:999–1007. Google Scholar

  11. B. F. Beal , M. R. Parker & K. W. Vencile . 2001. Seasonal effects of intraspecific density and predator exclusion along a shore-level gradient on survival and growth of juveniles of the soft-shell clam, Mya arenaria L. in Maine, USA. J. Exp. Mar. Biol. Ecol. 264:133–169. Google Scholar

  12. S. D. Beddingfield & J. B. McClintock . 2000. Demographic characteristics of Lytechinus variegatus (Echinodea: Echinodermata) from three habitats in a north Florida Bay, Gulf of Mexico. Mar. Ecol. (Berl.) 21:17–40. Google Scholar

  13. J. Bennett & A. C. Giese . 1955. The annual reproductive and nutritional cycles in two western sea urchins. Biol. Bull. 109:226–237. Google Scholar

  14. F. Berkes , T. P. Hughes , R. S. Steneck , J. A. Wilson , D. R. Bellwood , B. Crona , C. Folke , L. H. Gunderson , H. M. Leslie , J. Norerg , M. Nystrom , P. Olsson , H. Osterblom , M. Scheffer & B. Worm . 2006. Globalization, roving bandits, and marine resources. Science 311:1557–1558. Google Scholar

  15. F. R. Bernard 1977. Fishery and reproductive cycle of the red sea urchin, Strongylocentrotus franciscanus, in British Columbia. J. Fish. Res. Board Can. 34:604–610. Google Scholar

  16. G. Bigatti , E. M. Marzinelli , M. Cledon & P. E. Penchaszadeh . 2004. Gonadal cycle of Pseudechinus magellanicus (Philippi, 1857) (Echinoidea: Temnopleuridae) from Patagonia, Argentina. In: T. Heinzeller & J. H. Nebelsick , editors. Echinoderms: München. Proc. 11th Int. Echinoderm Conf., Leiden, The Netherlands: A. A. Balkema. pp. 11–14. Google Scholar

  17. J. J. Bisagni , D. J. Gifford & C. M. Ruhsam . 1996. The spatial and temporal distribution of the Maine Coastal Current during 1982. Cont. Shelf Res. 16:1–24. Google Scholar

  18. M. E. Blicher , S. Rysgaard & M.K. Sejr . 2007. Growth and production of sea urchin Strongylcentrotus droebaciensis in a high-Artic fjord, and growth along a climate gradient (64 to 77° N). Mar. Ecol. Prog. Ser. 341:89–102. Google Scholar

  19. R. A. Boolootian 1966. Reproductive physiology. In: R. A. Boolootian , editor. Physiology of echinodermata. New York: Interscience Publishers, John Wiley & Sons, Ltd. pp. 561–606. Google Scholar

  20. R. A. Boolootian & A. C. Giese . 1959. The effect of latitude on the reproductive activity of Strongylocentrotus purpuratus. In: M. Sears , editor. International Oceanographic Congress. Washington, DC: AAAS. pp. 216–217. Google Scholar

  21. R. A. Boolootian , A. C. Giese , J. S. Tucker & A. Farmanfarmaian . 1959. A contribution to the biology of a deep sea echinoid, Allocentrotus fragilis (Jackson). Biol. Bull. 116:362–372. Google Scholar

  22. S. M. Brady & R. E. Scheibling . 2006. Changes in growth and reproduction of green sea urchins, Strongylocentrotus droebachiensis (Müller), during repopulation of the shallow subtidal zone after mass mortality. J. Exp. Mar. Biol. Ecol. 335:277–291. Google Scholar

  23. P. A. Breen & K. H.Mann . 1976. Changing lobster abundance and the destruction of kelp beds by sea urchins. Mar. Biol. 34:137–142. Google Scholar

  24. P. E. Brewin , M. D. Lamare & J. A. Keogh . 2000. Reproductive variability over a four-year period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitats in New Zealand. Mar. Biol. 137:543–557. Google Scholar

  25. S. Brockington , L. S. Peck & P. A. Tyler . 2007. Gametogenesis and gonad mass cycles in the common circumpolar Antarctic echinoid Sterechinus neumayeri. Mar. Ecol. Prog. Ser. 330:139–147. Google Scholar

  26. M. I. Brogger , M. I. Martinez & P. E. Penchaszadeh . 2010. Reproduction of the sea urchin Arbacia dufresnii (Echinoidea: Arbaciidae) from Golfo Nuevo, Argentina. J. Mar. Biol. Assoc. U.K. 90:1405–1409. Google Scholar

  27. L. F. Bückle , C. Guisado , E. Tarifeño , A. Zuleta , L. Cordova & C. Serrano . 1978. Biological studies on the Chilean sea urchin Loxechinus albus (Molina) (Echinodermata: Echinodea) IV.Maturation cycle and seasonal biochemical changes in the gonad. Cienc. Mar. 5:1–19. Google Scholar

  28. M. Byrne 1990. Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar. Biol. 104:275–289. Google Scholar

  29. M. Byrne , N. L. Andrew , D. G. Worthington & P. A. Brett . 1998. Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Mar. Biol. 132:305–318. Google Scholar

  30. J. L. Catoira 1995. Spatial and temporal evolution of the gonad index of the sea urchin Paracentrotus lividus (Lamarck) in Galicia, Spain. In: R. Emson , A. Smith & A. Campbell , editors. Echinoderm research 1995. Rotterdam: A. A. Balkema. pp. 295–298. Google Scholar

  31. C. Chang-Po & C. Kun-Hsiung . 1981. Reproductive periodicity of the sea urchin, Tripneustes gratilla (L.) in Taiwan compared with other regions. Int. J. Invertebr. Reprod. 3:309–319. Google Scholar

  32. A. R. O. Chapman 1981. Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margaret's Bay, eastern Canada. Mar. Biol. 62:307–311. Google Scholar

  33. Y. Chen & M. Hunter . 2003. Assessing the green sea urchin (Strongylocentrotus droebachiensis) stock in Maine, USA. Fish. Res. 60:527–537. Google Scholar

  34. Y. Chen , M. Hunter , R. Vadas & B. Beal . 2003. Developing a growth transition matrix for the stock assessment of the green sea urchin (Strongylocentrotus droebachiensis) off Maine. Fish Bull. 101:737–744. Google Scholar

  35. B. Cocanour & K. Allen . 1967. The breeding cycles of a sand dollar and a sea urchin. Comp. Biochem. Physiol. 20:327–331. Google Scholar

  36. R. C. Cochran & F. Engelmann . 1975. Environmental regulation of the annual reproductive season of Strongylocentrotus purpuratus (Stimpson). Biol. Bull. 148:393–401. Google Scholar

  37. C. A. Comely & A. D. Ansell . 1989. The reproductive cycle of Echinus esculentus L. on the Scottish west coast. Estuar. Coast. Shelf Sci. 29:385–407. Google Scholar

  38. S. E. Coppard & A. C. Campbell . 2005. Lunar periodicities of diadematid echinoids breeding in Fiji. Coral Reefs 24:324–332. Google Scholar

  39. G. B. Crapp & M. E. Willis . 1975. Age determination in the sea urchin Paracentrotus lividus (Lamarck), with notes on the reproductive cycle. J. Exp. Mar. Biol. Ecol. 20:157–178. Google Scholar

  40. T. G. Dix 1970. Biology of Evechinus chloroticus (Echinoidea: Echinometridae) from different localities. N. Z. J. Mar. Freshwat. Res. 4:385–405. Google Scholar

  41. T. G. Dix 1977. Reproduction in Tasmanian populations of Heliocidaris erythrogramma (Echinodermata: Echinometridae). Aust. J. Mar. Freshwat. Res. 28:509–520. Google Scholar

  42. A. Dotan 1990. Reproduction of the slate pencil sea urchin, Heterocentrotus mammillatus (L.) in the northern Red Sea. Aust. J. Mar. Freshwat. Res. 41:457–465. Google Scholar

  43. A. E. Drummond 1991. Reproduction of the sea urchin Stompneustes variolaris (Lam.) on the east coast of South Africa. Invertebr. Reprod. Dev. 20:259–266. Google Scholar

  44. A. E. Drummond 1995. Reproduction of the sea urchins Echinometra mathaei and Diadema savignyi on the South African eastern coast. Mar. Freshwat. Res. 46:751–755. Google Scholar

  45. D. O. Duggins 1981. Sea urchins and kelp: the effects of short term changes in urchin diet. Limnol. Oceanogr. 26:391–394. Google Scholar

  46. C. P. Dumont , C. M. Pearce , C. Stazicker , A. Y. Xin & L. Keddy . 2006. Can photoperiod manipulation affect gonad development of a boreoarctic echinoid (Strongylocentrotus droebachiensis) following exposure in the wild after the autumnal equinox? Mar. Biol. 149:365–378. Google Scholar

  47. T. A. Ebert 1968. Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49:1075–1091. Google Scholar

  48. T. A. Ebert , J. C. Hernández & M. P. Russell . 2011. Problems of the gonad index and what can be done: analysis of the purple sea urchin Strongylocentrotus purpuratus. Mar. Biol. 158:47–58. Google Scholar

  49. T. A. Ebert , J. C. Hernández & M. P. Russell . 2012. Ocean conditions and bottom-up modifications of gonad development in the sea urchin Strongylocentotus purpuratus over space and time. Mar. Ecol. Prog. Ser. 467:147–167. Google Scholar

  50. R. Elmhirst 1923. Notes on the breeding and growth of marine animals in the Clyde Sea area. Annual Report. Scottish Marine Biological Association. pp. 19–43. Google Scholar

  51. R. H. Emson & P. G. Moore . 1998. Diet and gonad size in three populations of Echinus esculentus. In: R. Mooi & M. Telford , editors. Proceedings of the 9th International Echinoderm Conference, San Francisco, CA. Rotterdam: A. A. Balkema. pp. 641–644. Google Scholar

  52. H. Endo , N. Nakabayashi , Y. Agatsuma & K. Taniguchi . 2007. Food of the sea urchins Strongylocentrotus nudus and Hemicentrotus pulcherrimus associated with vertical distributions in fucoid beds and crustose coralline flats in northern Honshu, Japan. Mar. Ecol. Prog. Ser. 352:125–135. Google Scholar

  53. R. G. Ernest & N. J. Blake . 1981. Reproductive patterns within subpopulations of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea). J. Exp. Mar. Biol. Ecol. 55:25–37. Google Scholar

  54. I.-B. Falk-Peterson & S. Lönning . 1983. Reproductive cycles of two closely related sea urchin species, Strongylocentrotus droebachiensis (O. F. Müller) and Strongylocentrotus pallidus (G. O. Sars). Sarsia 68:157–164. Google Scholar

  55. L. Fenaux 1968. Maturation des gonades et cycle saisonnier des larves chez A. lixula, P. lividus et P. microtuberculatus (Echinides) à Villenfranche-sur-Mer. Vie Milieu 19:1–52. Google Scholar

  56. C. Fernandez 1998. Seasonal changes in the biochemical composition of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar. Ecol. (Berl.) 19:1–11. Google Scholar

  57. C. Fernandez & C. F. Boudouresque . 1997. Phenotypic plasticity of Paraocentrotus lividus (Echinodermata: Echinodea) in a lagoonal environment. Mar. Ecol. Prog. Ser. 152:145–154. Google Scholar

  58. S. A. Foo , S. A. Dworjanyn , A. G. B. Poore & M. Byrne . 2012. Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS One 7:e42497. Google Scholar

  59. H. M. Fox 1922. Lunar periodicity in reproduction. Nature 109:237–238. Google Scholar

  60. A. Fuji 1960a. Studies on the biology of the sea urchin III. Reproductive cycle of two sea urchins, Strongylocentrotus nudus and S. intermedius, in southern Hokkaido. Bull. Fac. Fish. Hokkaido Univ. 11:49–57. Google Scholar

  61. A. Fuji 1960b. Studies on the biology of the sea urchin I. Superficial and histological gonadal changes in gametogenic process of two sea urchins. Bull. Fac. Fish. Hokkaido Univ. 11:1–14. Google Scholar

  62. A. Fuji 1967. Ecological studies on the growth and food consumption of Japanese common littoral sea urchin, Strongylocentrotus intermedius. Mem. Fac. Fish. Hokkaido Univ. 15:83–160. Google Scholar

  63. H. Fujisawa 1989. Differences in temperature dependence of early development of sea urchins with different growing seasons. Biol. Bull. 176:96–102. Google Scholar

  64. H. Fujisawa & M. Shigei . 1990. Correlation of embryonic temperature sensitivity of sea urchins with spawning season. J. Exp. Mar. Biol. Ecol. 136:123–139. Google Scholar

  65. J. Gago , P. Range & O. J. Luis . 2003. Growth, reproductive biology and habitat selection of the sea urchin Paracentrotus lividus in the coastal waters of Cascais, Portugal. In: J. P. Féral & B. David , editors. Echinoderm research 2001. Lisse: A. A. Balkema. pp. 269–276. Google Scholar

  66. J. M. Garmendia , I. Menchaca , M. J. Belzunce , J. Franco & M. Revilla . 2010. Seasonal variability in gonad development in the sea urchin (Paracentrotus lividus) on the Basque coast (southeast Bay of Biscay). Mar. Pollut. Bull. 61:259–266. Google Scholar

  67. M. J. Garrido , R. J. Haroun & H. A. Lessios . 2000. Annual reproductive periodicity of the sea urchin Diadema antillarum Philippi in the Canary Islands. Bull. Mar. Sci. 67:989–996. Google Scholar

  68. C. Garside & J. C. Garside . 2004. Nutrient sources and distributions in Cobscook Bay. Northeast. Nat. (Steuben) 11:75–86. Google Scholar

  69. J. Gaudette , R. A. Wahle & J. H. Himmelman . 2006. Spawning events in small and large populations of the green sea urchin Strongylocentrotus droebaciensis as recorded using fertilization assays. Limnol. Oceanogr. 51:1485–1496. Google Scholar

  70. A. C. Giese 1959. Reproductive cycles of some west coast invertebrates. In: R. B. Withrow , editor. Photoperiodism and related phenomena in plants and animals, Publ. 55. Washington, DC: AAAS. pp. 625–638. Google Scholar

  71. A. C. Giese , L. Greenfield , H. Haung , A. Farmanfarmaian , R. Boolootian & R. Lasker . 1958. Organic productivity in the reproductive cycle of the purple sea urchin. Biol. Bull. 116:49–58. Google Scholar

  72. A. C. Giese , S. Krishnaswamy , B. S. Vasu & J. Lawrence . 1964. Reproductive and biochemical studies on a sea urchin, Stomopneustes variolaris, from Madras Harbor. Comp. Biochem. Physiol. 13:367–380. Google Scholar

  73. J. J. Gonor 1972. Gonad growth in the sea urchin, Strongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of gonad index methods. J. Exp. Mar. Biol. Ecol. 10:89–103. Google Scholar

  74. J. J. Gonor 1973a. Reproductive cycles in Oregon populations of the echinoid, Strongylocentrotus purpuratus (Stimpson) I. Annual gonad growth and ovarian gametogenic cycle. J. Exp. Mar. Biol. Ecol. 12:45–64. Google Scholar

  75. J. J. Gonor 1973b. Reproductive cycles in Oregon populations of the echinoid, Strongylocentrotus purpuratus (Stimpson) II. Seasonal changes in oocyte growth and in abundance. J. Exp. Mar. Biol. Ecol. 12:65–78. Google Scholar

  76. J. M. González-Irusta , F. Goni De Cerio & J. C. Canteras . 2010. Reproductive cycle of the sea urchin Paracentrotus lividus in the Cantabrian Sea (northern Spain): environmental effects. J. Mar. Biol. Assoc. U.K. 90:699–709. Google Scholar

  77. L. J. Grange , P. A. Tyler , L. S. Peck & N. Cornelius . 2004. Long-term interannual cycles of the gametogenic ecology of the Antarctic brittle star Ophionotus victoriae. Mar. Ecol. Prog. Ser. 278:141–155. Google Scholar

  78. A. Grant & P. A. Tyler . 1983. The analysis of data in studies of invertebrate reproduction I. Introduction and statistical analysis of gonad indices and maturity indicies. Int. J. Invertebr. Reprod. 6:259–269. Google Scholar

  79. P. J. Greenwood 1980. Growth, respiration and tentative energy budgets for two populations of the sea urchin Parechinus angulosus (Leske). Estuar. Coast. Mar. Sci. 10:347–367. Google Scholar

  80. M. Guettaf , G. A. San Martin & P. Francour . 2000. Interpopulation variability of the reproductive cycle of Paracentrotus lividus (Echinodermata: Echinoidea) in the south-western Mediterranean. J. Mar. Biol. Assoc. U.K. 80:899–907. Google Scholar

  81. M. Guillou & L. J. L. Lumingas . 1998. The reproductive cycle of the ‘blunt’ sea urchin. Aquacult. Int. 6:147–160. Google Scholar

  82. M. Guillou & L. J. L. Lumingas . 1999. Variation in the reproductive strategy of the sea urchin Sphaerechinus granularis (Echinodermata: Echinodea) related to food availability. J. Mar. Biol. Assoc. U.K. 79:131–136. Google Scholar

  83. M. Guillou & C. Michel . 1993. Reproduction and growth of Sphaerechinus granularis (Echinodermata: Echinoidea) in southern Brittany. J. Mar. Biol. Assoc. U.K. 73:179–192. Google Scholar

  84. M. Guillou & C. Michel . 1994. The influence of environmental factors on the growth of Sphaerechinus granularis (Lamarck) (Echinodermata: Echinoidea). J. Exp. Mar. Biol. Ecol. 178:97–111. Google Scholar

  85. N. T. Hagen , I. Jorgensen & E. S. Egeland . 2008. Sex-specific seasonal variation in the carotenoid content of sea urchin gonads. Aquat. Biol. 3:227–235. Google Scholar

  86. J. F. Hamel & A. Mercier . 1995. Spawning of the sea cucumber Cucumaria frondosa in the St. Lawrence Estuary, eastern Canada. SPC Beche-de-mer Bull. 7:12–21. Google Scholar

  87. L. H. Harrington , C. W. Walker & M. P. Lesser . 2007. Stereological analysis of nutritive phagocytes and gametogenic cells during the annual reproductive cycle of the green sea urchin, Strongylocentrotus drobachiensis. Invertebr. Biol. 126:202–209. Google Scholar

  88. E. B. Harvey 1956. The American Arbacia and other sea urchins. Princeton, NJ: Princeton University Press. 298 pp. Google Scholar

  89. Hemachandra & S. Thippeswamy . 2008. Allometry and condition index in green mussel Perna viridis (L.) from St. Mary's Island off Malpe, near Udupi, India. Aquacult. Res. 39:1747–1758. Google Scholar

  90. J. C. Hernández , A. Brito , N. García , M. C. Gil-Rodríguez , G. Herrera , A. Cruz-Reyes & J. M. Falcón . 2006. Spacial and seasonal variation of the gonad index of Diadema antillarum (Echinodermats: Echinodea) in the Canary Islands. Sci. Mar. 70:689–698. Google Scholar

  91. J. C. Hernández , S. Clemente & A. Brito . 2011. Effects of seasonality on the reproductive cycle of Diadema aff. antillarum in two contrasting habitats: implications for the establishment of a sea urchin fishery. Mar. Biol. 158:2603–2615. Google Scholar

  92. N. A. Hill , C. Blount , A. G. B. Poore , D. Worthington & P. D. Steinberg . 2003. Grazing effects of the sea urchin Centrostephanus rodgersii in two contrasting rocky reef habitats: effects of urchin density and its implications for the fishery. Mar. Freshwat. Res. 54:691–700. Google Scholar

  93. S. K. Hill & J. M. Lawrence . 2003. Habitats and characteristics of the sea urchins Lytechinus variegatus and Arbacia punctulata (Echinodermata) on the Florida Gulf-coast shelf. Mar. Ecol. (Berl.) 24:15–30. Google Scholar

  94. J. H. Himmelman 1975. Phytoplankton as a stimulus for spawning in three marine invertebrates. J. Exp. Mar. Biol. Ecol. 20:199–214. Google Scholar

  95. J. H. Himmelman 1978. Reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis. Can. J. Zool. 56:1828–1836. Google Scholar

  96. J. H. Himmelman 1999. Spawning, marine invertebrates. In: J. D. Neill , editor. Encyclopedia of reproduction. San Diego, CA: Academic Press. pp. 524–533. Google Scholar

  97. J. H. Himmelman , A. Cardinal & E. Bourget . 1983. Community development following removal of urchins, Strongylocentrotus droebachiensis, from the rocky subtidal zone of the St. Lawrence Estuary, eastern Canada. Oecologia 59:27–39. Google Scholar

  98. N. D. Holland 1967. Gametogenesis during the annual reproductive cycle in a cidaroid sea urchin (Stylocidaris affinis). Biol. Bull. 133:578–590. Google Scholar

  99. N. D. Holland & L. Z. Holland . 1969. Annual cycles in germinal and non-germinal cell populations in the gonads of the sea urchin Psammechinus microtuberculatus. Pubbl. Stn. Zool. Napoli 37:394–404. Google Scholar

  100. T. Horii 1997. The annual reproductive cycle and lunar spawning rhythms of the purple sea urchin Anthocidaris crassispina. Nippon Suisan Gakkaishi 63:17–22. Google Scholar

  101. J. A. Hutchings 1996. Spatial and temporal variation in the density of northern cod and a review of hypotheses for the stock's collapse. Can. J. Fish. Aquat. Sci. 53:943–962. Google Scholar

  102. T. M. Iliffe & J. S. Pearse . 1982.Annual and Lunar reproductive rhythms of the sea urchin, Diadema antillarum (Philippi) in Bermuda. Int. J. Invertebr. Reprod. 5:139–148. Google Scholar

  103. D. J. Jackson , S. M. Degnan & B. M. Degnan . 2012. Variation in rates of early development in Haliotis asinina generate competent larvae of different ages. Front. Zool. 9:2. Google Scholar

  104. A. -G. Jacquin , A. Donval , J. Guillou , S. Leyzour , E. Deslandes & M. Guillou . 2006. The reproductive response of the sea urchins Paracentrotus lividus (G.) and Psammechinus miliaris (L.) to a hyperproteinated macrophytic diet. J. Exp. Mar. Biol. Ecol. 339:43–54. Google Scholar

  105. P. J. James , P. Heath & M. J. Unwin . 2007. The effect of season, temperature and initial gonad condition on roe enhancement of the sea urchin Evechinus chloroticus. Aquaculture 270:115–131. Google Scholar

  106. D. W. Keats , R. G. Hooper , D. H. Steele & G. R. South . 1987. Field observations of summer and autumn spawning by Strongylocentrotus droebachiensis, green sea urchins, in eastern Newfoundland. Can. Field Nat. 101:463–465. Google Scholar

  107. D. W. Keats , G. R. South & D. H. Steele . 1984a. Ecology of juvenile green sea urchins (Strongylocentrotus droebachiensis) at an urchin dominated sublittoral site in eastern Newfoundland. In: B. F. Keegan & B. D. S. O'Connor , editors. Proceedings of the 5th International Echinoderm Conference, Galway, Ireland. Rotterdam: A. A. Balkema. pp. 295–302. Google Scholar

  108. D. W. Keats , D. H. Steele & G. R. South . 1983. Food relations in short term aquaculture potential of the green sea urchin (Strongylocentrotus droebachiensis) in New foundland. MSRL Tech. Rep.No. 24. pp. 1–24. Google Scholar

  109. D. W. Keats , D. H. Steele & G. R. South . 1984b. Depth-dependent reproductive output of the green sea urchin, Strongylocentrotus droebachiensis (O. F. Müller) in relation to the nature and availability of food. J. Exp. Mar. Biol. Ecol. 80:77–91. Google Scholar

  110. J. R. Kelly , K. A. Krumhansl & R. E. Scheibling . 2012. Drift algal subsidies to sea urchins in low-productivity habitats. Mar. Ecol. Prog. Ser. 452:145–157. Google Scholar

  111. M. S. Kelly 2000. The reproductive cycle of the sea urchin Psammechinus miliaris (Echinodermata: Echinoidea) in a Scottish sea loch. J. Mar. Biol. Assoc. U.K. 80:909–919. Google Scholar

  112. B. Kennedy & J. S. Pearse . 1975. Lunar synchronization of the monthly reproductive rhythm in the sea urchin Centrostephanus coronatus Verrill. J. Exp. Mar. Biol. Ecol. 17:323–331. Google Scholar

  113. C. K. King , O. Hoegh-Guldberg & M. Byrne . 1994. Reproductive cycle of Centrostephanus rodgersii (Echinoidea), with recommendations for the establishment of a sea urchin fishery in New South Wales. Mar. Biol. 120:95–106. Google Scholar

  114. S. Kino & Y. Agatsuma . 2007. Reproduction of sea urchin Loxechinus albus in Chiloé Island, Chile. Fish. Sci. 73:1265–1273. Google Scholar

  115. N. T. Kirchhoff , S. Eddy , N. P. Brown & N. Kobayashi . 2010. Out-ofseason gamete production in Strongylocentrotus droebachiensis: photoperiod and temperature manipulation. Aquaculture 103:77–85. Google Scholar

  116. N. Kobayashi 1969. Spawning periodicity of sea urchins at Seto III. Tripneustes gratilla, Echinometra mathaei, Anthocidaris crassipina and Echinostrephus aciculatus. Sci. Eng. Rev. Doshisha Univ. 9:254–269 (in Japanese with English abstract). Google Scholar

  117. N. Kobayashi & K. Nakamura . 1967. Spawning periodicity of sea urchins at Seto II. Diadema setosum. Publ. Seto Mar. Biol. Lab. 3:173–184. Google Scholar

  118. B. L. Kojis & N. J. Quinn . 1984. Seasonal and depth variation in fecundity of Acropora palifera at two reefs in Papua New Guinea. Coral Reefs 3:165–172. Google Scholar

  119. B. Konar 2001. Seasonal changes in subarctic sea urchin populations from different habitats. Polar Biol. 24:754–763. Google Scholar

  120. P. J. Krug 2009. Not my “Type”: larval dispersal dimorphisms and bethedging in opisthobranch life histories. Biol. Bull. 216:355–372. Google Scholar

  121. H. Kurihara , R. Yin , G. Nishihara , K. Soyana & A. Ishimatsu . 2013. Effect of ocean acidification on growth, gonad development and physiology of the sea urchin Hemicentrotus pulcherrimus. Aquat. Biol. 18:281–292. Google Scholar

  122. P. Laegdsgaard , M. Byrne & D. T. Anlefson . 1991. Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Mar. Biol. 110:359–374. Google Scholar

  123. M. D. Lamare 1998. Origin and transport of larvae of the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in aNew Zealand fiord. Mar. Ecol. Prog. Ser. 174:107–121. Google Scholar

  124. M. D. Lamare , P. E. Brewin , M. F. Barker & S. R. Wing . 2002. Reproduction of the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. N. Z. J. Mar. Freshwat. Res. 36:719–732. Google Scholar

  125. M. Lamare & B. Stewart . 1998. Mass spawning by the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in aNew Zealand fiord. Mar. Biol. 132:135–140. Google Scholar

  126. C. Lang & K. H. Mann . 1976. Changes in sea urchin populations after the destruction of kelp beds. Mar. Biol. 36:321–326. Google Scholar

  127. B. R. Larson , R. L. Vadas & M. Keser . 1980. Feeding and nutritional ecology of the sea urchin Strongylocentrotus drobachiensis in Maine, USA. Mar. Biol. 59:49–62. Google Scholar

  128. R. Lasker & A. C. Giese . 1954. Nutrition of the sea urchin, Strongylocentrotus purpuratus. Biol. Bull. 106:328–340. Google Scholar

  129. J. M. Lawrence 1975. On the relationships between marine plants and sea urchins. Oceanogr. Mar. Biol. Annu. Rev. 13:213–286. Google Scholar

  130. J. M. Lawrence , A. L. Lawrence & N. D. Holland . 1965. Annual cycle in the size of the gut of the purple sea urchin, Strongylocentrotus purpuratus (Stimpson). Nature 205:1238–1239. Google Scholar

  131. C. D. Lefèvre & D. R. Bellwood . 2011. Temporal variation in coral reef ecosystem process: herbivory of macroalgae by fishes. Mar. Ecol. Prog. Ser. 422:239–251. Google Scholar

  132. M. Lemire & J. H. Himmelman . 1996. Relation of food preference to fitness for the green sea urchin, Strongylocentrotus droebachiensis. Mar. Biol. 127:73–78. Google Scholar

  133. V. Leoni , C. Fernandez , M. Johnson , L. Ferrat & C. Pergent-Martini . 2003. Preliminary study on spawning periods in the sea urchin Paracentrotus lividus. In: J. P. Féral & B. David , editors. Echinoderm research 2001. Lisse: A. A. Balkema. pp. 277–280. Google Scholar

  134. H. A. Lessios 1981. Reproductive periodicity of the Echinoids Diadema and Echinometra on the two coasts of Panama. J. Exp. Mar. Biol. Ecol. 50:47–61. Google Scholar

  135. H. A. Lessios 1985. Annual reproductive periodicity in eight echinoid species on the Caribbean coast of Panama. In: B. F. Keegan & B.D. S. O °Connor , editors. Proceedings of the 5th International Echinoderm Conference, Galway, Ireland. Rotterdam: A. A. Balkema. pp. 303–311. Google Scholar

  136. H. A. Lessios 1991. Presence and absence of monthly reproductive rhythms among eight Caribbean echinoids off the coast of Panama. J. Exp. Mar. Biol. Ecol. 153:27–47. Google Scholar

  137. S. E. Lester , S. D. Gaines & B. P. Kinlan . 2007. Reproduction on the edge: large-scale patterns of individual performance in a marine invertebrate. Ecology 80:22–39. Google Scholar

  138. L. A. Levin , H. Caswell , K. D. DePatra & E. L. Creed . 1987. Demographic consequences of larval development mode: planktotrophy vs. lecithotrophy in Streblospio benedicti. Ecology 68:1877–1886. Google Scholar

  139. D. R. Levitan 1988a. Asynchronous spawning and aggregative behavior in the sea urchin Diadema antillarum (Philippi). In: R. Burke , editor. Proceedings of the 6th International Echinoderm Conference on Echinoderm Biology. Rotterdam: A. A. Balkema Press. pp. 181–186. Google Scholar

  140. D. R. Levitan 1988b. Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76:627–629. Google Scholar

  141. D. R. Levitan 1989. Density-dependent size regulation in Diadema antillarum effects on fecundity and survivorship. Ecology 70:1414–1424. Google Scholar

  142. J. B. Lewis 1958. The biology of the tropical sea urchin Tripneustes esculentus Leske in Barbados, British West Indies. Can. J. Zool. 36:607–621. Google Scholar

  143. J. B. Lewis 1966. Growth and breeding in the tropical Echinoid Diadema antillarum Philippi. Bull. Mar. Sci. 16:151–158. Google Scholar

  144. J. B. Lewis & G. S. Storey . 1984. Differences in morphology and life history traits of the echinoid Echinometra lucunter from different habitats. Mar. Ecol. Prog. Ser. 15:207–211. Google Scholar

  145. E. J. Lima , P. B. Gomes & J. R. Souza . 2009. Reproductive biology of Echinometra lucunter (Echinodermata: Echinoidea) in a northeast Brazilian sandstone reef. An. Acad. Bras. Cienc. 81:51–59. Google Scholar

  146. S. D. Ling , C. R. Johnson , S. Frusher & C. K. King . 2008. Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Global Change Biol. 14:907–915. Google Scholar

  147. M. M. Littler & D. S. Littler . 1980. The evolution of thallus from and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am. Nat. 116:25–44. Google Scholar

  148. E. Low-Décarie , C. Chivers & M. Granados . 2014. Rising complexity and falling explanatory power in ecology. Front. Ecol. Environ 12:412–418. Google Scholar

  149. S. López , X. Turon , E. Montero , C. Palacin , C. M. Duarte & I. Tarjuelo . 1998. Larval abundance, recruitment and early mortality in Paracentrotus lividus (Echinoidea). interannual variability and plankton-benthos coupling. Mar. Ecol. Prog. Ser. 172:239–251. Google Scholar

  150. J. Lozano , J. Galera , S. Lopez , X. Turon , C. Palacin & G. Morera . 1995. Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar. Ecol. Prog. Ser. 122:179–191. Google Scholar

  151. R. B. MacFarlane & E. C. Norton . 1999. Nutritional dynamics during embryonic development in the viviparous genus Sebastes and their application to the assessment of reproductive success. Fish Bull. 97:273–281. Google Scholar

  152. N. Mahdavi Shahri , Z. Haghighat Khazaei , S. Karamzadeh , F. Naseri , A. A. Esteki & H. Rameshi . 2008. Reproductive cycle of the sea urchin Echinometra mathaei (Echinodermatidea: Echinoidea) in Bostaneh, Persian Gult, Iran. J. Biol. Sci. 8:1138–1148. Google Scholar

  153. Maine Department of Marine Resources (DMR). 2014. Commercial fisheries landings. Available at:  http://www.maine.gov/dmr/commercialfishing/documents/urchin.table.pdfGoogle Scholar

  154. F. L. F. Mariante , G. B. Lemos , F. J. Eutrópio & L. C. Gomes . 2009. Reproductive biology of Echinometra lucunter (Echinodermata: Echinoidea) in Praia da Costa, Vila Velha, Espírito Santo. Zoologia 26:641–646. Google Scholar

  155. I. Martínez , F. J. Garcia , A. I. Sanchez , J. L. Daza & F. del Castillo . 2003. Biometric parameters and reproductive cycle of Paracentrotus lividus (Lamarck) in three habitats of Southern Spain. In: J. P. Féral & B. David , editors. Echinoderm research 2001. Lisse: A. A. Balkema. pp. 281–287. Google Scholar

  156. I. Martínez-Pita , A. I. Sanchez-Espana & F. J. Garcia . 2008. Gonadal growth and reproduction in the sea urchin Sphaerechinus granularis (Lamarck 1816) (Echinodermata: Echinoidea) in southern Spain. Sci. Mar. 72:603–611. Google Scholar

  157. E. M. Marzinelli , G. Bigatti , J. Gimenez & P. E. Penchaszadeh . 2006. Reproduction of the sea urchin Pseudechinus Magellanicus (Echinoidea: Temnopleuridae) from Golfo Nuevo, Argentina. Bull. Mar. Sci. 79:127–136. Google Scholar

  158. R. Masuda & J. C. Dan . 1977. Studies on the annual reproductive cycle of the sea urchin and the acid phosphatase activity of relict ova. Biol. Bull. 153:577–590. Google Scholar

  159. T. Matsui , Y. Agatsuma , M. Ogasawara & K. Taniguchi . 2008. Coincidence in reproduction of the sea urchin Strongylocentrotus intermedius in Hirota Bay, on the Pacific Ocean of northern Honshu, and in the Sea of Japan off Hokkaido, Japan. J. Shellfish Res. 27:1283–1289. Google Scholar

  160. D. A. McCarthy & C. M. Young . 2002. Gametogenesis and reproductive behavior in the echinoid Lytechinus variegatus. Mar. Ecol. Prog. Ser. 233:157–168. Google Scholar

  161. J. D. McGillicuddy Jr. , V. K. Kosnyrev , J. P. Ryan & J. A. Yoder . 2001. Covariation of mesoscale ocean color and sea-surface temperature patterns in the Sargasso Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 48:1823–1836. Google Scholar

  162. R. A. McKinney , S. M. Glatt & S. R. McWilliams . 2004. Allometric length-weight relationships for benthic prey of aquatic wildlife in coastal marine habitats. Wildl. Biol. 10:241–249. Google Scholar

  163. B. F. McPherson 1965. Contributions to the biology of the sea urchin Tripneustes ventricosus. Bull. Mar. Sci. 15:228–244. Google Scholar

  164. B. F. McPherson 1968. Contributions to the biology of the sea urchin Eucidaris tribuloides (Lamarck). Bull. Mar. Sci. 18:400–443. Google Scholar

  165. B. F. McPherson 1969. Studies on the biology of the tropical sea urchins, Echinometra lucunter and Echinometra viridis. Bull. Mar. Sci. 19:195–213. Google Scholar

  166. P. E. McShane , P. K. Gerring , O. A. Anderson & R. A. Stewart . 1996. Population differences in the reproductive biology of Evechinus chloroticus (Echinodea: Echinometridae). N. Z. J. Mar. Freshwat. Res. 30:333–339. Google Scholar

  167. S. K. Meidel & R. E. Scheibling . 1998. Annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis, in differing habitats in Nova Scotia, Canada. Mar. Biol. 131:461–478. Google Scholar

  168. S. K. Meidel & R. E. Scheibling . 1999. Effects of food type and ration on reproductive maturation and growth of the sea urchin Stongylocentrotus droebachiensis. Mar. Biol. 134:155–166. Google Scholar

  169. R. J. Miller 1997. Spatial differences in the productivity of American lobster in Nova Scotia. Can. J. Fish. Aquat. Sci. 54:1613–1618. Google Scholar

  170. R. J. Miller & K. H.Mann . 1973. Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. III. Energy transformations by sea urchins. Mar. Biol. 18:99–114. Google Scholar

  171. M. A. Minor & R. E. Scheibling . 1997. Effects of food ration and feeding regime on growth and reproduction of the sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 129:159–167. Google Scholar

  172. M. F. Montero-Torreiro & P. Garcia-Martinez . 2003. Seasonal changes in the biochemical composition of body components if the sea urchin Paracentrotus lividus, in Lorbé (Galicia, north-western Spain). J. Mar. Biol. Assoc. U.K. 83:575–581. Google Scholar

  173. H. B. Moore 1934.Acomparison of the biology of Echinus esculentus in different habitats. Part I. J. Mar. Biol. Assoc. U.K. 19:869–886. Google Scholar

  174. H. B. Moore 1936. The biology of Echinocardium cordatum. J. Mar. Biol. Assoc. U.K. 20:655–671. Google Scholar

  175. H. B. Moore , T. Jutare , J. C. Bauer & J.A. Jones . 1963a. The biology of Lytechinus variegatus. Bull. Mar. Sci. Gulf Caribb. 13:23–53. Google Scholar

  176. H. B. Moore , T. Jutare, J. A. Jones , B. F. McPherson & C. F. E. Roper . 1963b. A contribution to the biology of Tripneustes eculentus. Bull. Mar. Sci. Gulf Caribb. 13:267–281. Google Scholar

  177. H. B. Moore & N. N. Lopez . 1972. Factors controlling variation in the seasonal spawning pattern of Lytechinus variegatus. Mar. Biol. 14:275–280. Google Scholar

  178. L. E. Morgan , L. W. Botsford , S. R. Wing & B.D. Smith . 2000. Spatial variability in growth and mortality of the red sea urchin, Strongylocentrotus franciscanus, fishery in northern California. Can. J. Fish. Aquat. Sci. 57:980–992. Google Scholar

  179. T. Mori , T. Tsuchiya & S. Amemiya . 1980. Annual gonadal variation in sea urchins of the orders Echinothurioida and Echinoida. Biol. Bull. 159:728–736. Google Scholar

  180. J. E. Munk 1992. Reproduction and growth of green urchins Strongylocentrotus droebachiensis (Müller) near Kodiak, Alaska. J. Shellfish Res. 11:245–254. Google Scholar

  181. N. A. Muthiga 2003. Coexistence and reproductive isolation of the sympatric echinoids Diadema savignyi (Michelin) and Diadema setosum (Leske) on Kenyan coral reefs. Mar. Biol. 143:669–677. Google Scholar

  182. N. A. Muthiga 2005. Testing for the effects of seasonal and lunar periodicity on the reproduction of the edible sea urchin Tripneustes gratilla (L) in Kenyan coral reef lagoons. Hydrobiologia 549:57–64. Google Scholar

  183. N. A. Muthiga & V. Jaccarini . 2005. Effects of seasonality and population density on the reproduction of the Indo-Pacific Echinoid Echinometra mathaei in Kenyan coral reef lagoons. Mar. Biol. 146:445–453. Google Scholar

  184. National Marine Fisheries Service. 2014. Annual commercial landing statistics. Available at:  http://www.st.nmfs.noaa.gov/commercialfisheries/commercial-landings/annual-landings/indexGoogle Scholar

  185. S. A. Navarette , E. A. Wieters , B. R. Broitman & J. C. Castilla . 2005. Scales of benthic-pelagic coupling and intensity of species interactions: from recruitment limitation to top-down control. Proc. Natl. Acad. Sci. USA 102:18046–18051. Google Scholar

  186. D. Nichols , G. M. Bishop & A. A. T. Sime . 1985. Reproductive and nutritional periodicities in populations of the European sea-urchin, Echinus esculentus (Echinodermata: Echinoidea) from The English Channel. J. Mar. Biol. Assoc. U.K. 65:203–220. Google Scholar

  187. C. O'Connor , G. Riley , S. Lefebvre & D. Bloom . 1978. Environmental influences on histological changes in the reproductive cycle of four New South Wales sea urchins. Aquaculture 15:1–17. Google Scholar

  188. S. A. Oganesyan 1998. Reproductive cycle of the echinoid Strongylocentrotus droebachiensis in the Barents Sea. In: R. Mooi & M. Telford , editors. Echinoderms. Proceedings of the 9th International Echinoderm Conference, San Francisco, CA. pp. 765–768. Google Scholar

  189. M. Ogasawara , T. Matsui & Y. Agatsuma . 2011. Growth and rapid gonad recovery of the sea urchin Hemicentrotus pulcherrimus after spawning in an Undaria pinnatifida and Saccharina japonica kelp bed. J. Shellfish Res. 30:159–166. Google Scholar

  190. J. H. Orton 1929. On the occurrence of Echinus esculentus on the foreshore in the British Isles. J. Mar. Biol. Assoc. U.K. 16:289–296. Google Scholar

  191. R. Ouréns , L. Fernández , M. Fernández -Boán , I. Naya & J. Freire . 2013. Reproductive dynamics of the sea urchin Paracentrotus lividus on the Galicia coast (NW Spain): effects of habitat and population density. Mar. Biol. 160:2413–2423. Google Scholar

  192. R. Ouréns , L. Fernández & J. Freire . 2011. Geographic, population, and seasonal patterns in the reproductive parameters of the sea urchin Paracentrotus lividus. Mar. Biol. 158:793–804. Google Scholar

  193. R. Ouréns , J. Freire & L. Fernández . 2012. Definition of a new unbiased gonad index for aquatic invertebrates and fish: its application to the sea urchin Paracentrotus lividus. Aquat. Biol. 17:145–152. Google Scholar

  194. S. T. Oyarzún , S. L. Marín , C. Valladares & J. L. Iriarte . 1999. Reproductive cycle of Loxechinus albus (Echinodermata: Echinoidea) in two areas of the Magellan Region (53° S, 70–72° W), Chile. Sci. Mar. 63(Suppl. 1):439–449. Google Scholar

  195. G. C. Packard & T. J. Boardman . 1999. The use of percentages and sizespecific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp. Biochem. Physiol. 122:37–44. Google Scholar

  196. J. S. Pearse 1968. Patterns of reproductive periodicities in four species of Indo-Pacific echinoderms. Proc. Indiana Acad. Sci. 68:247–279. Google Scholar

  197. J. S. Pearse 1969a. Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez I. The echinoids Prionocidaris baculosa (Lamarck) and Lovenia elongata (Gray). Bull. Mar. Sci. 19:323–350. Google Scholar

  198. J. S. Pearse 1969b. Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez II. The echinoid Echinometra mathaei (De Blanville). Bull. Mar. Sci. 19:580–613. Google Scholar

  199. J. S. Pearse 1970. Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez III. The echinoid Diadema setosum (Leske). Bull. Mar. Sci. 20:697–720. Google Scholar

  200. J. S. Pearse 1972. A monthly reproductive rhythm in the diadematid sea urchin Centrostephanus coronatus Verrill. J. Exp. Mar. Biol. Ecol. 8:167–186. Google Scholar

  201. J. S. Pearse & B. F. Phillips . 1968. Continuous reproduction in the Indo-Pacific sea urchin Echinometra mathaei at Rottnest Island, Western Australia. Aust. J. Mar. Freshwat Res. 19:161–172. Google Scholar

  202. D. Pecorino , M. D. Lamare & M. F. Barker . 2013. Reproduction of the Diadematidae sea urchin Centrostephanus rodgersii in a recently colonized area of northern New Zealand. Mar. Biol. Res. 9:157–168. Google Scholar

  203. J. T. Pennington 1985. The ecology of fertilization of Echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol. Bull. 169:417–430. Google Scholar

  204. A. F. Pérez , C. Boy , E. Morriconi & J. Calvo . 2010. Reproductive cycle and reproductive output of the sea urchin Loxechinus albus (Echinodermata: Echinodea) from Beagle Channel, Tierra del Fuego, Argentina. Polar Biol. 33:271–280. Google Scholar

  205. A. F. Pérez , E. Morriconi , C. Boy & J. Calvo . 2008. Seasonal changes in energy allocation to somatic and reproductive body components of common cold temperature sea urchin Loxechinus albus in a sub-Antarctic environment. Polar Biol. 31:443–449. Google Scholar

  206. T. Platt , L. M. Dickie & R. W. Trites . 1970. Spatial heterogeneity of phytoplankton in a near-shore environment. J. Fish. Res. Board Can. 27:1453–1473. Google Scholar

  207. S. M. Quijano & A. G. Gaspar . 2005. Reproductive cycle of Lytechinus variegatus (Echinoidea: Toxopneustidae) in the south of Margarita Island, Venezuela. Rev. Biol. Trop. 53:305–312. Google Scholar

  208. J. E. Randall , R. E. Schroeder & W. A. Starck II . 1964. Notes on the biology of the echinoid Diadema antillarum. Caribb. J. Sci. 4:421–433. Google Scholar

  209. S. R. Rodriguez 2003. Consumption of drift kelp by intertidal populations of the sea urchin Tetrapygus niger on the central Chilean coast: possible consequences at different ecological levels. Mar. Ecol. Prog. Ser. 251:141–151. Google Scholar

  210. M. P. Russell 1998. Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus droebachiensis (Müller). J. Exp. Mar. Biol. Ecol. 220:1–14. Google Scholar

  211. A. I. Sánchez-España , I. Martínez-Pita & F. J. García . 2004. Gonadal growth and reproduction in the commercial sea urchin Paracentrotus lividus (Lamarck, 1816) (Echinodermata: Echinoidea) from southern Spain. Hydrobiologia 519:61–72. Google Scholar

  212. E. Sanford & D. J. Worth . 2009. Genetic differences among populations of a marine snail drive geographic variation in predation. Ecology 90:3108–3118. Google Scholar

  213. R. E. Scheibling & B. G. Hatcher . 2001. The ecology of Strongylocentrotus droebachiensis. In: J. M. Lawrence , editor. Edible sea urchins: biology and ecology. New York: Elsevier. pp. 353–392. Google Scholar

  214. R. E. Scheibling & A. W. Hennigar . 1997. Recurrent outbreaks of disease in sea urchins Strongylocentrotus droebachiensis in Nova Scotia: evidence for a link with large-scale meteorologic and oceanographic events. Mar. Ecol. Prog. Ser. 152:155–165. Google Scholar

  215. A. Schuhbauer , P. Brickle & A. Arkhipkin . 2010. Growth and reproduction of Loxechinus albus (Echinodermata: Echinoidea) at the southerly peripheries of their species range, Falkland Islands (South Atlantic). Mar. Biol. 157:1837–1847. Google Scholar

  216. F. Sellem & M. Guillou . 2007. Reproductive biology of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats of northern Tunisia (south-east Mediterranean). J. Mar. Biol. Assoc. U.K. 87:763–767. Google Scholar

  217. L. C. N. Seward 2002. The relationship between green sea urchin spawning, spring phytoplankton blooms, and the winter-spring hydrography at selected sites in Maine. M.S. Thesis, University of Maine, Orono, ME. Google Scholar

  218. N. M. Shahri , Z. H. Khazaei , S. Karamzadeh , F. Naseri , A. A. Esteki & H. Rameshi . 2008. Reproductive cycle of the sea urchin Echinometra mathaei (Echinodermatidea: Echinoidea) in Bostaneh, Persian Gulf, Iran. J. Biol. Sci. 8:1138–1148. Google Scholar

  219. K. Sivertsen & C. C. E. Hopkins . 1995. Demography of the echinoid Strongylocentrotus droebachiensis related to biotope in northern Norway. In: H. R. Skjoldal , C. Hopkins , K. E. Erikstad & H. P. Leinaas , editors. Proceedings of Mare Nor Symposium Ecology of fjords and coastal waters, Tromsø, Norway, 5–9 December 1994. Amsterdam: Elsevier Science B.V. pp. 549–571. Google Scholar

  220. R. R. Sokal & F. J. Rohlf . 1981. Biometry, 2nd edition. New York: W. H. Freeman and Company. 859 pp. Google Scholar

  221. D. Soualili & M. Guillou . 2009. Variation in the reproductive cycle of the sea urchin Paracentrotus lividus in three differently polluted locations near Algiers (Algeria). Mar. Biodivers. Rec. 2:1–6. Google Scholar

  222. C. Spirlet , P. Grosjean & M. Jangoux . 1998. Reproductive cycle of the echinoid Paracentrotus lividus: analysis by means of maturity index. Invertebr. Reprod. Dev. 34:69–81. Google Scholar

  223. D. Stanwell-Smith & L. S. Peck . 1998. Temperature and embryonic development in relation to spawning and field occurrence of larvae of three Antarctic echinoderms. Biol. Bull. 194:44–52. Google Scholar

  224. M. Starr , J.H. Himmelman & J. C. Therriault . 1990. Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247:1071–1074. Google Scholar

  225. M. Starr , J. H. Himmelman & J. C. Therriault . 1992. Isolation and properties of a substance from the diatom Phaeodactylum tricornutum which induces spawning in the sea urchin Strongylocentrotus droebachiensis. Mar. Ecol. Prog. Ser. 79:275–287. Google Scholar

  226. M. Starr , J. H. Himmelman & J. C. Therriault . 1993. Environmental control of green sea urchin, Strongylocentrotus droebachiensis, spawning in the St. Lawrence Estuary. Can. J. Fish. Aquat. Sci. 50:894–901. Google Scholar

  227. R. G. D. Steele & J. H. Torrie . 1980. Principles and procedures of statistics: a biomedical approach. 2nd edition. New York: McGraw-Hill Book Co. 633 pp. Google Scholar

  228. R. S. Steneck & M. N. Dethier . 1994. A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498. Google Scholar

  229. R. S. Steneck , M. H. Graham , B. J. Bourque , D. Corbett , J. M. Erlandson , J. A. Estes & M. J. Tegner . 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29:436–459. Google Scholar

  230. R. E. Stephens 1972. Studies on the development of the sea urchin Strongylocentrotus droebachiensis I. Ecology and normal development. Biol. Bull. 142:132–144. Google Scholar

  231. F. C. Stott 1931. The spawning of Echinus esculentus and some changes in gonad composition. J. Exp. Biol. 8:133–150. Google Scholar

  232. M. Stumpp , K. Trubenbach , D. Brennecke , M. Y. Hu & F. Melzner . 2012. Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat. Toxicol. 110–11:194–207. Google Scholar

  233. G. Thorson 1950. Reproduction and larval ecology of marine bottom invertebrates. Biol. Rev. Camb. Philos. Soc. 25:1–45. Google Scholar

  234. S. Tomšić , A. Conides , I. Dupčić-Radić & B. Glamuzina . 2010. Growth, size class frequency and reproduction of purple sea urchin, Paracentrotus lividus (Lamarck, 1816) in Bistrina Bay (Adriatic Sea, Croatia). Acta Adriat. 51:67–77. Google Scholar

  235. D. W. Townsend , N.D. Rebuck , M. A. Thomas , L. Karp-Boss & R.M. Gettings . 2010. A changing nutrient regime in the Gulf of Maine. Cont. Shelf Res. 30:820–832. Google Scholar

  236. G. C. Trussell & R. J. Etter . 2001. Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail. Genetica 112–113:321–337. Google Scholar

  237. A. Y. Tuason & E. D. Gomez . 1979. The reproductive biology of Tripneustes gratilla Linnaeus (Echinoidea: Echinodermata) with some notes on Diadema setosum Leske. Proceedings of the International Symposium on Marine Biogeography and Evolution in Southern Hemisphere, vol. 2. Wellington, NZ: N. Z. Dept. Sci. Indust. Res. pp. 707–716. Google Scholar

  238. P. A. Tyler & J. D. Gage . 1984. Seasonal reproduction of Echinus affinis (Echinodermata: Echinodea) in the Rockall Trough, northeast Atlantic Ocean. Deep-Sea Res. 31:387–402. Google Scholar

  239. A. J. Underwood , M. G. Chapman & S. D. Connell . 2000. Observations in ecology: you can't make progress on processes without understanding the patterns. J. Mar. Biol. Ecol. 250:87–115. Google Scholar

  240. A. J. Underwood & M. J. Keough . 2001. Supply-side ecology: the nature and consequences of variation in recruitment of intertidal organisms. In: M. D. Bertness , S. D. Gaines & M. E. Hay , editors. Marine community ecology. Sunderland, MA: Sinauer Associates, Inc. pp. 201–220. Google Scholar

  241. R. L. Vadas 1977. Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47:337–371. Google Scholar

  242. R. L. Vadas 1992. Littorinid grazing and algal patch dynamics. In: J. Grahame , P. J. Mill & D. G. Reid , editors. Proceedings of the 3rd International Symposium on Littorinid Biology. London: The Malacological Society of London. pp. 197–209. Google Scholar

  243. R. L. Vadas & B. L. Beal . 1999. Temporal and spatial variability in the relationships between adult size, maturity and fecundity in green sea urchins: the potential use of a roe-yield standard as a conservation tool. Report to the Maine Department of Marine Resources, Augusta, ME. 47 pp. Google Scholar

  244. R. L. Vadas , B. Beal , T. Dowling & J. C. Fegley . 2000. Experimental field tests of natural algal diets on gonad index and quality in the green sea urchin, Strongylocentrotus droebachiensis: a case for rapid summer production in post-spawned animals. Aquaculture 182:115–135. Google Scholar

  245. R. L. Vadas , B. Beal , S. Dudgeon & W. Wright . 1997. Reproductive biology of green sea urchins along the coast of Maine: final report. Orono, ME: Maine Sea Grant. 43 pp. Google Scholar

  246. R. L. Vadas & W. S. Grant . 1973. Feeding and reproductive biology of an estuarine population of the sea urchin, Strongylocentrotus droebachiensis. Bull. Ecol. Soc. Am. 54:34. Google Scholar

  247. R. L. Vadas , B. D. Smith , B. Beal & T. Dowling . 2002. Sympatric growth morphs and size bimodality in the green sea urchin (Strongylocentrotus droebachiensis). Ecol. Monogr. 72:113–132. Google Scholar

  248. D. Vaïtilingon , R. Rasolofonirina & M. Jangoux . 2005. Reproductive cycle of edible echinoderms from the southwestern Indian Ocean I. Tripneustes gratilla L. (Echinoidea, Echinodermata). Western Indian Ocean J. Mar. Sci. 4:47–60. Google Scholar

  249. M. A. Vaschenko, P.M. Zhadan & E. V. Latypova . 2001. Long-term changes in the state of gonads in sea urchins Strongylocentrotus intermedius from Amur Bay, the Sea of Japan. Russ. J. Ecol. 32:358–364. Google Scholar

  250. E. Vasseur 1952. Geographic variation in the Norwegian sea-urchins, Strongylocentrotus droebachiensis and S. pallidus. Evolution 6:87–100. Google Scholar

  251. C. R. R. Ventura , R. S. Varotto , A. L. P. S. Carvalho , A. D. Pereira , S. L. Alves & F. S. MacCord . 2003. Interpopulation comparison of the reproductive and morphological traits of Echinometra lucunter (Echinodermata: Echinoidea) from two different habitats on Brazilian coast. In: J. P. Féral and B. David , editors. Echinoderm research 2001. Lisse: A. A. Balkema. pp. 289–293. Google Scholar

  252. G. I. Viktorovskaya & V. I. Matveev . 2000. Relation between the time of reproduction of the sea urchins Strongylocentrotus intermedius and the water temperature of the northern Primoré coast. Oceanology (Mosc.) 40:73–78. Google Scholar

  253. G. I. Viktorovskaya & Y. I. Zuenko . 2005. The impact of environmental conditions on the reproduction of the sea urchin Strongylocentrotus pallidus (Sars) off the Primoré coast, Japan Sea. Oceanology (Mosc.) 45:76–84. Google Scholar

  254. R. A. Wahle & S. H. Peckham . 1999. Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis. Mar. Biol. 134:127–137. Google Scholar

  255. C. W. Walker & M. P. Lesser . 1998. Manipulation of diet and photoperiod can promote out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: important implications for land-based aquaculture. Mar. Biol. 132:663–676. Google Scholar

  256. M. M. Walker 1982. Reproductive periodicity in Evechinus chloroticus in the Hauraki Gulf. N. Z. J. Mar. Freshwat. Res. 16:19–25. Google Scholar

  257. O. S. Wangensteen , X. Turon , M. Casso & C. Palacín . 2013. The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod. Mar. Biol. 8 pp. doi: 10.1007/s00227-013-2303-8. Google Scholar

  258. J. E. Williamson & P. D. Steinberg . 2002. Reproductive cycle of the sea urchin Holopneustes purpurascens (Temnopleuridae: Echinodermata). Mar. Biol. 140:519–532. Google Scholar

  259. B. J. Winer , D. R. Brown & K. M. Michels . 1991. Statistical principles in experimental design. 3rd edition. New York: McGraw-Hill. 1057 pp. Google Scholar

  260. D. G. Worthington & C. Blount . 2003. Research to develop and manage the sea urchin fisheries of NSW and Eastern Victoria. Fisheries Research and Development Corporation, Report No. 99/128. Sydney, Australia: Fisheries Research and Development Corporation. Google Scholar

  261. K. Yatsuya & H. Nakahara . 2004. Density, growth and reproduction of the sea urchin Anthocidaris crassispina (A. Agassiz) in two different adjacent habitats, the Sargassum area and Corallina area. Fish. Sci. 70:233–240. Google Scholar

  262. C. M. Young , P. A. Tyler , J. L. Cameron & S. G. Rumrill . 1992. Seasonal breeding aggregations in low-density populations of the bathyal echinoid Stylocidaris lineata. Mar. Biol. 113:603–612. Google Scholar

  263. S. Zamora & W. Stotz . 1992. Ciclo reproductivo de Loxechinus albus (Molina 1782) (Echinodermata: Echinoidea) en Punta Lagunillas, IV Region, Coquimbo, Chile. Rev. Chil. Hist. Nat. 65:121–133. Google Scholar

  264. S. Zamora & W. Stotz . 1993. Ciclo reproductivo de Tetrapygus niger (Molina 1782) (Echinodermata: Echinoidea) en dos localidades de la IV Region, Coquimbo, Chile. Rev. Chil. Hist. Nat. 66:155–169. Google Scholar

Robert L. Vadas Sr., Brian F. Beal, Steven R. Dudgeon, and Wesley A. Wright "Spatial and Temporal Variability of Spawning in the Green Sea Urchin Strongylocentrotus droebachiensis along the Coast of Maine," Journal of Shellfish Research 34(3), 1097-1128, (1 September 2015). https://doi.org/10.2983/035.034.0337
Published: 1 September 2015
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