A life history model for the San Francisco Estuary population of the Chinese mitten crab, Eriocheir sinensis (Decapoda: Grapsoidea)

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1 Biological Invasions (2) 7: Ó Springer 2 A life history model for the San Francisco Estuary population of the Chinese mitten crab, Eriocheir sinensis (Decapoda: Grapsoidea) Deborah Rudnick 1,7, Tanya Veldhuizen 2, Richard Tullis 3, Carolyn Culver 4, Kathryn Hieb & Brian Tsukimura 6, * 1 University of California, Berkeley, California, USA; 2 California Department of Water Resources, Sacramento, California, USA; 3 California State University, Hayward, California, USA; 4 University of California at Santa Barbara, California, USA; California Department of Fish and Game, Stockton, California, USA; 6 Department of Biology, California State University (CSU), Fresno, California, USA; 7 Present address:, Years Institute, Bainbridge Island, Washington, USA; *Author for correspondence ( briant@csufresno.edu; fax: ) Received 24 July 23; accepted in revised form June 24 Key words: catadromous, Chinese mitten crab, crustacea, Eriocheir, estuary, invasive, life history model, San Francisco Bay Abstract First discovered in San Francisco Bay in 1992, the Chinese mitten crab, Eriocheir sinensis, has become established over hundreds of km 2 of the San Francisco Estuary. Ecological and economic impacts of this invasive species motivated our search for a greater understanding of the crab s life history as an important step in better management and control. Data for this life history model comes from the authors research and scientific literature. Juvenile crabs migrate from the Estuary into fresh water where they develop into adults. Environmental signals may stimulate gonad development that is followed by a downstream migration beginning at the end of summer. Mating occurs after the crabs reach saline water. Embryos are carried until hatching, and the larvae undergo five zoeal stages before settlement. Our model projects rates of development at various temperatures and growth increments, supports a minimum of 2 years in low salinity or freshwater habitat, and predicts that most California mitten crabs are at least 3 years old before becoming sexually mature. Environmental factors strongly influence the timing and duration of the crab s life stages, and are discussed in the context of a gradient of development times for worldwide populations of this important invasive species. Introduction The Chinese mitten crab, Eriocheir sinensis (Decapoda: Grapsoidea), was first detected in San Francisco Estuary in A population explosion of mitten crabs occurred in the Estuary in 1998, prompting widespread concern about this species potential impacts. Native to rivers and estuaries of the west coast of North Korea south to Shanghai, China, invasive populations of E. sinensis also exist throughout freshwater and estuarine systems of central and western Europe as a result of introductions over the past century (Hoestlandt 1948; Haahtela 1963; Ingle 1986; Ja_zd_zewski and Konopacka 1993; Dhur and Massard 199; Clark et al. 1998; Cabral and Costa 1999; Gollasch 1999). Introduced populations of the Chinese mitten crab have caused several economic and ecological impacts. Commercial and recreational fishing operations have been hindered by bait stealing and damage to gear and the catch by the crab (Panning 1939a; Rudnick and Resh 22). In California, the mitten crab has also interfered with operations at federal and state water diversion plants and power plants (Siegfried 1999;

2 334 Veldhuizen and Stanish 1999). The burrowing habit of E. sinensis has undermined the integrity of stream banks and levees throughout its introduced range (Peters and Panning 1933; Dutton and Conroy 1998), particularly in south San Francisco Estuary watersheds (Rudnick et al. 23). The mitten crab likely impacts freshwater and estuarine food webs at many levels, as it has an opportunistic diet that includes algae, detritus, and a variety of benthic macroinvertebrates (Panning 1939a; Hoestlandt 1948; Gollasch 1999; Rudnick and Resh in review). These impacts have been, and likely will continue to be, exacerbated by population explosions such as was seen in 1998 in San Francisco Estuary; similar rapid fluctuations in abundance have been reported from several European countries (Panning 1939a; Gollasch 1999; Herborg et al. 23). Research conducted on populations of the mitten crab underscores the spatial and temporal variability of this species life history across its global distribution. For example, E. sinensis are reported to take 3 years to reach sexual maturity in northern Europe (Panning 1939a; Gollasch 1999), while 1 2 years to maturity has been reported for southern and central China (Hymanson et al. 1999; Zhang et al. 21). There are substantial differences in crab abundance among populations throughout the world; for example, periodically massive abundances are found in Germany and England (Clark et al. 1998; Gollasch 1999), while relatively small populations have persisted in several countries such as Finland and Poland (Haahtela 1963; Ja_zd_zewski and Konopacka 1993). Efforts to understand the ecology of the mitten crab and control its impacts in California have been hindered by an incomplete understanding of the population dynamics of this species. Increased understanding of the factors that drive mitten crab abundance and distribution could help scientists and managers better predict and prepare for years with high abundance. For example, the 1998 mitten crab population explosion lead to near-total mortality of fish and greatly increased handling and engineering costs at the US Bureau of Reclamation pumping facility and fish bypass tanks in tributaries to San Francisco Estuary (Siegfried 1999). Improving predictive power for the population dynamics of this species could help better prepare for years of high crab abundance and reduce impacts on wildlife and water supply. A greater understanding of the factors that control abundance and distribution can also inform our understanding of the preferred habitats and geographic limits of distribution of this species, improving risk assessment for future invasions of the crab. Using the scientific literature available for this species and data we have collected, we present a discussion of the life history of the San Francisco Estuary population of the Chinese mitten crab. The model is organized into four developmental stages (larva, megalopa, juvenile, and adult), with discussions of the physiological and ecological requirements and preferences that characterize each stage. We supplement our data for the San Francisco Estuary population of the crab (Table 1) with published data from native and introduced populations, and examine similarities and differences across these data sets, discussing environmental factors that may shape these differences. Our discussion is focused primarily on the seasonal timing and distributional patterns of the four life stages of the crab as a foundation for building the life history model. After the life stages are discussed, we describe a model based on data about larval development and juvenile growth rates to estimate time to sexual maturity for the San Francisco Estuary population of the mitten crab. Our discussion and model identifies factors that may assist in predicting the population dynamics of the mitten crab, and outlines areas that warrant additional research to solidify our understanding of mitten crab life history. Study system The San Francisco Estuary (N 37 4, W ), which includes South San Francisco Bay, central San Francisco Bay, San Pablo Bay (we refer to the latter two areas collectively as North San Francisco Bay ), Suisun Bay and Marsh, and the Sacramento San Joaquin Delta (the Delta), forms the largest estuary (approximately 16 mi 2 ) on the west coast of North America, draining about 4% (3, km 2 ; 4 million acres) of California s surface area (Nichols et al. 1986; Hymanson et al. 1994) (Figure 1). The Estuary is a large, tidal, and highly modified ecosystem (Nichols et al. 1986). About 9% of the Estuary s freshwater inflow originates from the

3 33 Table 1. California data sets contributing to the development of the Chinese mitten crab life history model. Reference (if previously published data) Type of data Research location Primary researcher Institution Period of data collection Crab life stage Larvae Growth rates Laboratory R. Tullis California State University Hayward Juveniles Growth rates Laboratory R. Tullis California State University Hayward Growth rates San Francisco Bay and T. Veldhuizen California Department of Water Sacramento/San Joaquin Delta Resources Abundance and South San Francisco Bay C. Culver University of California Santa 21 Culver and Walter size distribution Barbara (22) Growth rates and South San Francisco Bay D. Rudnick University of California Berkeley 2 21 size distribution Laboratory B. Tsukimura California State University Fresno 2 23 Toste (21), Bauer and Tsukimura (22) Adults Reproductive development Rudnick et al. (23) California Department of Fish and Game/Department of Water Resources/US Bureau of Reclamation K. Hieb and S. Foss San Francisco Bay and Sacramento/San Joaquin Delta Adult abundance and morphology Delta watershed (SFEP 1992). The region is characterized as having a Mediterranean climate with cool, wet winters (November April) and warm, dry summers (May October) (SFEP 1992). On average, Estuary temperatures range from about C in winter to 2 C in summer (Herrgesell et al. 1983; USGS 23). The Chinese mitten crab encounters a mosaic of physical and chemical conditions throughout the San Francisco Estuary. South San Francisco Bay is a large (4 km 2 ), shallow bay with an average depth of 3 m and silt and clay sediments (SFEP 1992). Salinities in the South Bay range from 3& in the Bay to approximately & at tributary mouths. South Bay water temperatures range between about C in winter to 23 C in summer, and are often slightly (1 3 ) warmer than temperatures in the central and north bays (USGS 23). Tidal influence extends 8 km up tributaries (Rudnick et al. 23) that are shallow, short (< km), and drain small steep watersheds with very short lag times and high peak runoffs. To the north, San Pablo Bay is a large (272 km 2 ), shallow bay characterized by expansive tidal mudflats. To the east of San Pablo Bay, salinities in the dredged channels and shoals of Suisun Bay are highly variable in response to changes in freshwater outflow from the Sacramento-San Joaquin Delta (Herrgesell et al. 1983), and range from approx..2 to.6& (Hymanson et al. 1994). The tidal and freshwater habitats of the Sacramento San Joaquin Delta (2978 km 2 ) is the confluence of several major rivers; depths range from <1 to m in shallow open water to > m in channels, and annual mean salinities range from.6 to 2.27& (Hymanson et al. 1994). Water temperatures in the Delta range between about C in winter to 2 C in summer (Herrgesell et al. 1983), but some regions of the Delta can reach 2 C during summer months (DWR 21). Materials and methods Data supplying the model and life history discussion Information used to generate the life history model includes data published about native and introduced populations of the mitten crab, and

4 336 were maintained as individuals in individual finger bowls with the same water conditions and fed salmon pellets (Nelson & Sons suppliers) and Egeria densa, an aquatic macrophyte. Carapace width (CW) of juvenile mitten crabs was measured within a few hours following each molt using Vernier calipers at the widest part of the carapace between the fourth anterolateral teeth. Time until the first member of the group transitioned to the subsequent stage or molt (minimum time to stage) was recorded for Zoea II, II, and V, the megalopa, and the first 14 juvenile molts. Figure 1. Distribution of the Chinese mitten crab, in bold black, in the San Francisco Estuary in 21. Reports and sightings of the crabs from individuals and monitoring programs used to generate this distribution map were compiled and synthesized by the CA Department of Fish and Game. Juvenile sampling sites indicated in the three areas in which data was collected to support the time to maturity model: sampling in the Delta conducted by T. Veldhuizen; sampling on Coyote Creek conducted by C. Culver; and sampling on Calabazas Creek conducted by D. Rudnick. published and unpublished data from the authors research (Table 1). Here, we describe methods for research that has not previously been published and was used to develop the life history model: (1) larval and juvenile growth rates of mitten crabs raised in the laboratory; (2) juvenile crab recruitment patterns documented in a South Bay tributary; and (3) incremental growth rates of juveniles in the field. Larval and juvenile growth rates Mitten crab eggs were harvested from six gravid females collected from the Delta and bred in the laboratory at California State University, Hayward. Upon hatching, all eggs were combined. The resulting larva were maintained in finger bowls containing 2 3 individuals kept at 2& at 17 C and fed Artemia nauplii. The juveniles Juvenile crab recruitment and size patterns In order to collect data on abundance and sizes of newly settled mitten crabs, recruitment collectors were placed in the high tidal portion ( & salinity) of Coyote Creek, Santa Clara County, CA (Figure 1). Three sets of collectors were deployed at the site in mid-january because it was unlikely that mitten crab larvae would be present earlier in the season (see life history discussion below), and were removed mid-august when settlement of decapods had not been detected for two consecutive months. Each set of collectors consisted of four dish scrub pads (Tuffy Ò ) attached to a weighted polypropylene line approximately 1 m from the bottom of the line. Collectors were retrieved and replaced 2 per month. Retrieved collectors were placed in plastic bags and frozen until processing. Samples were thawed in the laboratory and examined under a microscope for crab megalopae and juveniles. All crabs were identified to species and enumerated. Carapace width (CW) of mitten crabs was measured either microscopically (crabs < mm) or using Vernier calipers (crabs > mm). Juvenile mitten crabs were also collected in the upper tidal portion of Calabazas Creek, a tributary to South San Francisco Bay, by D. Rudnick using artificial shelter traps with a set time of approximately 2 weeks, between November 2 and October 21 (Rudnick 23; Veldhuizen 23). This passive trap is composed of multiple stacked tubes (6 in. diameter) that are used as shelter by the juvenile crabs. This substrate offers larger refugia than the Tuffy collectors described above, and a range of larger crabs was correspondingly collected in these tube traps. Collected crabs were measured (CW) and sexed (can

5 337 be determined for crabs >7 mm CW (Rudnick 23)). Incremental growth rates of juvenile crabs Mitten crabs were collected in Calabazas Creek, a tributary to South San Francisco Bay, and in lowsalinity tributaries to the Sacramento San Joaquin Delta (Figure 1) using artificial shelter traps with a set time of approximately 2 weeks, as described above. Molts were assumed to belong to crabs captured in the same trap when those crabs were soft-shelled or appeared to have recently molted (light-colored setae on chelae, no epiphytic growth), were slightly larger in size (within mm carapace width (CW)), and of the same sex. CW of crabs and molts was taken between the fourth anterolateral teeth using Vernier calipers. Ten pairs of recently molted crabs (2 4 mm CW) and their molts were collected in Calabazas Creek, South San Francisco Bay, between November 2 and October 21. Six recently molted crabs (19 49 mm CW) and molts were collected in the Delta from August 2 to July 21. Linear regression was used to determine the relationship between pre- and post-molt sizes. Because of these small sample sizes, we did not test for significant differences between the molting rates from these two data sets, but rather used the resulting range of values as a way of adding a measure of variability to our model. Development of time-to-maturity estimates We developed a model of the time span for mitten crabs to reach sexual maturity from hatching. To construct the model, we used information about larval development rates with growth rate data for juvenile mitten crabs. To incorporate information about growth rate variability, we used multiple growth rates under varying temperatures, salinities, and habitats from our field and laboratory studies. Estimates of time to maturity are a function of: (1) Timing of larval hatching. We used three hatching times: December 1, March 1, and July 1, as these times cover the range of the estimated mitten crab breeding period. (2) Rates of larval development under varying temperatures. We used Anger s (1991) larval development rates, because these rates were relatively consistent with our laboratory data, and provided more information about development rates under multiple temperatures and salinities. We used lower water temperatures, of 12 and C, to guide time of development for early- and mid-season hatched larvae, as these temperatures are appropriate to Bay conditions during the winter and spring, while higher temperatures ( 18 C) were used for late-hatching larvae that develop in the warmer spring and summer temperatures of San Francisco Bay (USGS 23). (3) Molting rates for young juvenile mitten crabs raised in the laboratory. A function describing the time between molts was generated from the growth rate curve developed from this data. (4) Incremental growth rate, or the increase of body size during a single molt. These data were derived from crabs raised in the laboratory for newly settled juvenile crabs, and for larger crabs ( 2 mm CW) collected in the field in South San Francisco Bay and in the Delta. Larval development rates were generated by starting with one of the three hatching dates, then adding time to metamorphosis based on temperature. The rate of growth of the first year juvenile was modeled by starting with a 2 mm CW (newly settled juvenile as determined from laboratory studies and confirmed by field data) crab and, using our data for the frequency of molting and growth increments of young crabs, generating estimates of the amount of growth a juvenile could achieve in its first year of life. Rates of incremental growth generated from two sets of field data for older juvenile crabs were used to estimate rates of growth for crabs larger than 2 mm CW. By combining the data for time from hatching to metamorphosis with growth rate data through the first year and up to sizes consistent with sizes of sexually mature crabs collected from San Francisco Bay, we established estimates for total time for mitten crabs to reach maturity from hatching. Results and discussion Life history of the Chinese mitten crab Larvae There have been few collections of mitten crab larvae from the San Francisco Estuary; therefore,

6 338 hatching is inferred from the timing of the presence of ovigerous females. The majority of ovigerous female Chinese mitten crabs occur between November and March in the open waters of the San Francisco Estuary, with smaller numbers of ovigerous females collected from April to June (Rudnick et al. 23). Female mitten crabs have extruded multiple broods in the laboratory; however, subsequent broods contained lower numbers of viable eggs (C. Culver and R. Tullis, unpublished data). Under laboratory conditions in California, eggs of E. sinensis hatched in approximately 3 days at 17 C and 2& salinity, but have been reported to take longer (or developing more slowly) at lower temperatures in other laboratory experiments (Anger 1991) (Table 2). In the cold waters of northern Europe, embryonic development may be slowed, so that females hold on to fertilized eggs through the winter, moving to shallower, warmer waters in the spring, where the larvae are released (Ingle 1986). Among other decapod crustacea, there is also evidence for delays in development and maintenance of eggs until favorable conditions commence for hatching (Sastry 1983; Adiyodi 198). It is unknown if delays in egg development and hatching occur for the San Francisco Estuary population of the crab. If development is not delayed for ovigerous females early in the reproductive season, eggs could feasibly hatch as early as the beginning of December. Overall, the period of egg production and development in the San Francisco Estuary spans November to June (Table 3). Mitten crab eggs hatch into free-swimming pelagic larvae. E. sinensis typically has five larval stages (Zoeae I V) (Kim and Hwang 1994; Montu et al. 1996). Mitten crab larvae are euryhaline; however, they still require at least 16 17& salinity to survive in the intermediate zoeal stages in the laboratory (Anger 1991). Zoeae I have a larger capacity to tolerate lower salinities than intermediate stages (Anger 1991; R. Tullis, pers. obs.). These changes in salinity preferences support a mitten crab larval association with the brackish water of estuaries at hatching, followed by transport of the larvae away from shore by currents to higher salinity waters during later larval stages (Anger 1991). This pattern of movement has been reported for other brachyuran crustacean larvae that are exported to the coastal ocean (Garvine et al. 1997; Epifanio and Garvine 21). However, it is unknown whether mitten crab larvae undergo coastal export, or if a larval retention mechanism might help them remain in the estuary. Water temperature likely influences both survival and rate of development of mitten crab larvae. Anger s (1991) laboratory data indicated that higher salinities and temperatures were correlated with faster rates of development, with time to megalopal stage ranging between 18 and 74 days (Table 2). Mitten crabs raised in aquaculture conditions in China at 23 C passed through each zoeal stage in 2 4 days, completing larval development in about days (Zhao 1988). Our data suggest a longer time to development than found in Anger s data (Table 2); part of this variation may be due to the fact that we used slightly lower salinities than those used by Anger, who detected slightly faster development rates in early larval stages with higher salinities (2&) (1991). Temperatures below 9 C were lethal to larvae in German laboratory experiments (Anger 1991), yet the crab s distribution in Northern Europe includes waters that are regularly colder than this temperature (Anger 1991). Thus, the lethal limit may be lower in nature than has been indicated by laboratory studies. Megalopae The megalopa is the post-larval stage that occurs prior to settling of the crab as a benthic juvenile. Mitten crab megalopae have been suggested to use tidal currents to move into river systems from the estuary (Panning 1939b). Active migration towards less saline waters has been described for other megalopae in the grapsoid superfamily to which mitten crabs belong (Ryan and Choy 199). In the laboratory, megalopae show signs of increased tolerance to low salinities (Anger 1991), and those raised in the laboratory in California tolerated fresh to low salinity water of & (R. Tullis, pers.obs.). In natural habitats, megalopae have been collected in low salinity ( &) areas throughout the world (Schnakenbeck 1933 as cited in Anger 1991; Panning 1939a; Ingle 1986; Jiang Dinhe, pers. comm., Culver and Walter 22). Thus, as hypothesized by Panning (1939a) and Anger (1991), the megalopal stage is likely responsible

7 339 Table 2. Rates of larval and post-larval development as a function of salinity and temperature. Larval stage R. Tullis data Anger (1991) Minimum number of days to stage at 17 C, 2 ppt salinity Salinity a at 12 C b : optimal c (total range withstood) Days at 12 C and 2 ppt: mean value d Salinity at C: optimal (total range withstood) Days at C and 2 ppt: mean value Salinity at 18 C: optimal (total range withstood) Zoea I n.d ( 32) ( 32) ( 32) Zoea II n.d ( 32) ( 32) ( 32) Zoea III ( 32) ( 32) ( 32) Zoea IV ( 32) ( 32) ( 32) Zoea V n.d (2 32) (2 32) ( 32) Time to megalopa Megalopa 21 None (2 32) 18 (2 2) (2 32) 2 32 Total days to metamorphosis Days at 18 C and 2 ppt: mean value First column is our data (R. Tullis); remaining columns are data summarized from Anger a Salinities tested by Anger were 32& in & increments. b Temperatures tested were 6,9,12, and 18 C; temperatures of 6 and 9 C did not allow for survival beyond Zoea I. c Optimal conditions are those with the highest percent survival obtained among the salinities tested at the given temperature. For Zoeae I IV, the highest survival rates were >6% at the salinity shown; for Zoea, >%, and for Megalopa, >4% (Anger 1991). d Confidence intervals could not be translated from graphic data; in general, confidence intervals for these values ranged from ±.1 to ±. days.

8 34 Table 3. Comparisons of select aspects of the timing and conditions of the life history of the Chinese mitten crab in its native and introduced ranges. Region Extent of range First record of species General estuarine temperatures (winter summer) China a N Native 8 27 C (Yangtze) W. Europe b Germany Period of larval settlement Size of sexually mature adults Collected (mm CW) April June 38 9 (aquaculture: some as small as 3) Period of downstream migration August November (September) 2 4 N C May August August October France N C April July 9 August October England (Thames) Breeding period c : range (peak if known) October to April (December) Years of population peak abundance n.d.; low since 196s October May ; 3 6; 69 7; 79 83; n.d. 194s (no. France), Late 19s (so. France) 1. N C n.d. n.d. n.d. n.d. Early 199s n.d. California 37 4 N C April June +? 3 9 August December Data sources Cohen and Weinstein (21), Hymanson et al. (1999) Panning (1939), Hoestlandt (1948), Herborg et al. (23) Cohen and Weinstein (21), USGS (23) Panning (1939), Hymanson et al. (1999), this paper Hoestlandt (1948), Jin et al. (1999); Zhang et al. (21), Rudnick et al. (23) Hymanson et al. (1999), Gollasch (1999), Hoestlandt (1948), Rudnick et al. (23), Herborg et al. (23) November June (December February) Panning (1939a, b), Hymanson et al. (1999), Rudnick et al. (23) Suggested life span 1 3 years 4 6 years n.d years; average may be 3 Gollasch (1999), Cohen and Weinstein (21), Rudnick et al. (23), this paper Panning (1939a, b), Hymanson et al. (1999), this paper a Data for wild populations comes primarily from the Yangtze River (28 32 N); additional data as noted from aquacultured mitten crab populations raised primarily in ponded conditions). b Range of the mitten crab includes several other European countries, including Poland, The Netherlands, Czechoslovakia Portugal, and Spain (See Rudnick et al. 23); the three countries chosen are those for which substantial life history data was found. c Breeding period includes mating and the period in which eggs are carried by the female until hatching.

9 341 for movement towards lower salinity water in preparation for metamorphosis into a benthic juvenile. Movement towards low salinity habitat during the pelagic stage of this organism may be affected by outflow during the period of migration. Little is known about the effects of increased freshwater outflow on the retention of zooplankton (Kimmerer et al. 22). If megalopae have some ability to cue towards freshwater sources, higher flows may attract more crabs, leading to a positive correlation between settling and discharge. However, high flows could also delay or reduce success of upstream migration of these very small organisms by preventing megalopae and young benthic crabs from reaching the habitat required for their development. One finding that supports the latter hypothesis is that the only collections of megalopae (n ¼ 3) in South San Francisco Bay occurred in April simultaneously with a substantial decline in water discharge that had not been seen since January of that year (Culver and Walter 22). Studies of an invasive population of the Chinese mitten crab in the UK suggested a correlation between long-term declines in discharge from freshwater systems with increased abundance of this species (Atrill and Thomas 1996). However, as water temperature and salinity are also affected by flow, additional information is needed to decipher the potential influence of these factors on mitten crab settlement. There has been minimal research conducted examining the timing or location of San Francisco Estuary mitten crab megalopae. One mitten crab megalopa was collected in North San Francisco Bay as early as February (K. Hieb, pers. obs.) and a few were collected in April in two tributaries of South San Francisco Bay (Culver and Walter 22). As larvae likely hatch as late as early summer (see larval section above), mitten crab megalopae probably occur into the summer. Panning (1939a) reported that in Germany, where winter and spring conditions are much cooler and wetter than California, megalopae settle in July/August in warmer years, but not until October during cooler/wetter years. Juveniles Age crabs. Age crabs are defined for the purpose of this life history model as juveniles between their date of metamorphosis and the start of the following calendar year. Age crabs begin as the initial crab-like form that follows from the pelagic megalopa. The newly settled juvenile crab is benthic and initially resides in water between 1 and 2& salinity (Culver and Walter 22; Rudnick et al. 23). The carapace width (CW) of newly metamorphosed juveniles raised in the laboratory from San Francisco Estuary larvae is 2 3 mm, similar to sizes reported for newly settled mitten crabs in other countries (Panning 1939a; Montu et al. 1996). These recently settled juveniles were collected over a large temporal distribution (April June) in a South San Francisco Bay tributary (Figure 2). Young mitten crabs molt frequently, approximately every 2 weeks for the first 8 molts in the laboratory at 17 C (Figure 3). Similar to other brachyuran crustacea (Hartnoll 1982), the rate of molting decreases as mitten crabs grow 3 2 < mm -mm >mm Number of crabs 2 1/29/21 2/28/21 3/3/21 4/29/21 /29/21 6/28/21 7/28/21 8/27/21 Figure 2. Number of juvenile mitten crabs of three size classes collected biweekly between January and August 21 on Coyote Creek, a tributary to South San Francisco Bay. Data provided by C. Culver.

10 342 Days from start of juvenile life stage mal growth was reported for a Chinese population of Chinese mitten crabs between January and July, with molting rates increasing during the warm summer months (Jin et al. 21). As temperatures in freshwater tributaries to San Francisco Bay drop in the autumn, mitten crabs may slow or cease growing in the winter. It has been suggested that mitten crabs remain in brackish habitats through their first winter, and do not commence migration into fresh water until the following year (Panning 1939a). In California, young juveniles (< mm) are found in tidally influenced, low salinity (1 %) habitats (Culver and Walter 22; Rudnick et al. 23). On a few occasions, small crabs (<7 mm CW) have been collected in fresh water in the eastern Sacramento San Joaquin Delta, 4 6 km upstream of North San Francisco Bay (Veldhui-.2782(days to molt N) days to molt N+1 = 8.834e R 2 = size after each molt (mm CW) Figure 3. An exponential equation fitted to growth rate data for the first 13 molts of juvenile Chinese mitten crabs raised in the laboratory at approx. 17 C. Molting dates are based on the date on which the first individual of the juvenile cohort (n ¼ approx. crabs) molted to the next stage. Data provided by R. Tullis. larger (Figure 3; Zhang et al. 21). The incremental growth rate of San Francisco Estuary juvenile mitten crabs raised in the laboratory averaged 22% CW increase per molt (Figure 4). The distribution of sizes of early staged crabs from natural habitats supports the occurrence of a molt increment around 22% in South Bay tributaries (C. Culver, unpublished data), and is similar to increments reported for small crabs in Germany (24%) (Panning 1939a).This molt increment is similar to growth rates reported for other young juvenile grapsoid crabs (Spivak 1988; Luppi et al. 22) and other decapods (Hartnoll 1982). The growth rate of the young juvenile mitten crab likely has a direct relationship to water temperature, with colder temperatures lengthening the intermolt period, as has been reported for other brachyuran crustacea (Hartnoll 1982). Mini new CW (mm) new CW = (old CW) R 2 = old CW (mm) Figure 4. Relationship of pre- and post-molt sizes (carapace width) of juvenile mitten crabs. (a) (n ¼ ) collected from Calabazas Creek, South San Francisco Bay. (b) (n ¼ 6) collected from North San Francisco Bay. Correlation provides an estimated 18% growth rate for the South Bay population of mitten crabs, and 26% growth rate for North Bay population of mitten crabs.

11 343 New CW (mm) (a) New CW (mm) (b) new CW = (old CW) R 2 = Old CW (mm) New CW = (Old CW) R 2 = Old CW (mm) Figure. Relationship of pre- and post-molt sizes (carapace width) of juvenile mitten crabs. (a) (n=) collected from Calabazas Creek, South San Francisco Bay. (b) (n ¼ 6) collected from North San Francisco Bay. Correlation provides an estimated 18% growth rate for the South Bay population of mitten crabs, and 26% growth rate for North Bay population of mitten crabs. zen 23). For the most part, however, juveniles smaller than mm CW are not found in freshwater habitats. Age 1 crabs. For this life history model, Age 1 crabs hatched during the previous calendar year (plus December of the year before, if hatched very early in the previous reproductive season). By this time, the crab is readily identified as male or female, as their abdominal shape is clearly differentiated (D. Rudnick, T. Veldhuizen, pers. obs.). In both sexes the setae on the chelae, from which the common name mitten crab derives, are evident. Our field studies documented molt increments of approximately 18% in crabs between 2 and 4 mm collected from tributaries to South San Francisco Bay (Figure a), and about 26% among similarly sized crabs collected from the Sacramento/San Joaquin Delta (Figure b). Studies of Chinese populations of the mitten crab have reported the increase in carapace width per molt (the growth increment) between 13 and 26% for crabs between 21 and 63 mm CW (Kamps 1939 as cited in Zhang 21). Juvenile mitten crabs begin their movement into freshwater habitat at a size consistent with model estimates for the crabs at the beginning of age 1 (approx. 3 mm CW, see time to maturity model below). This upstream migration may be rapid (1 3 km/day) (Panning 1939a). Little is known about the cues that initiate this migration. Environmental cues may include temperature or increasing day length (following the winter solstice). Upstream migration could be triggered by increases in water flow (Gollasch 1999). Others have suggested that crab density and food quality/quantity may influence upstream migration of juvenile crabs, such that no upstream migration occurs if crab densities are low and food availability is high (Panning 1939a; Ingle 1986). Sampling in tidally influenced (1 &) South Bay tributaries has procured some large (4 mm plus) crabs throughout the summer and fall that may be older crabs that never left this habitat (Figure 6). In California, actively upstream-migrating crabs were collected in the tributaries upstream of the Delta from mid-january through mid-march during the population boom in 1998 (K. Hieb, pers. obs.). Small (approximately 2 mm CW) crabs and molts have been collected in South San Francisco Bay tributaries at least km upstream from of the Bay in May and June (Rudnick 23), suggesting that age 1 crabs move into freshwater habitat by late spring. Age 2+ crabs. Our size models estimate that mitten crabs range in size from 2 49 mm CW at the beginning of age 2 (see time to maturity model below). Crabs in this size range collected from both North and South Bay watersheds are characterized by several morphological changes associated with progression to sexual maturity, including: increased growth of setae on the walking legs, increase in fullness of the mittens of setae on the front claws, particularly in males; in females, setae begin to form around the outer edge of the abdomen and the abdomen becomes more rounded and fills in a larger portion of the

12 344 Frequency // Carapace Width (mm) /28/ /3/ /1/ /13/ /29/ /1/ /2/ /19/ /17/ // /31/ Figure 6. Histograms of carapace widths of Chinese mitten crabs collected by passive traps between December 2 and August 21 in Calabazas Creek, a tributary to South San Francisco Bay. Storm events precluded sampling in January March. Data provided by D. Rudnick. underside of the carapace; and in males, the sperm ducts become fully developed and clearly visible when the abdomen is lifted away from the carapace (Hoestlandt 1948; Rudnick 23). Little is known about the growth rate of age 2 mitten crabs in California. It has been suggested that the intermolt period increases and growth increment decreases as the crab ages; in Germany, incremental growth rates of small juveniles averaged 24%, but crabs 7 mm in carapace length (similar to CW) had a molt increment of only 11% (Panning 1939a; size of the smaller juveniles was not reported). Panning (1939a) also reported a decline in molting frequency, from 6 to 8 times during their first year [= our Age 1 crabs], 4 to times during their second year, and 2 to 3 times during their third the older crabs shed only once a year (pp ). Decreased molt increments and increased molt intermolt periods typically occur with increasing size of decapod crustaceans (e.g., Hartnoll 1982; Seiple and Salmon 1987; Luppi et al. 22). Adults Before downstream migration to the breeding ground commences, mitten crabs gonads begin to develop. Females raised in ponds in China have been shown to undergo ovarian development prior to migration (Zhang et al. 21), and dissections of female mitten crabs collected from freshwater tributaries to the San Francisco Estu-

13 34 ary indicate ovarian development prior to the start of migration (Toste 21). The environmental cues that might stimulate gonad maturation are not yet described. Preliminary data indicates that shorter day lengths (following the summer solstice) stimulate ovarian development (Toste 21). In China, summer rain results in increased water flow and lower water temperatures, and these factors may play a role in triggering gonad development. However, in California, these meteorological phenomena occur in fall and winter, by which time the crabs have achieved sexual maturity. Initiation of reproductive development may also be size-dependent. In preliminary tests, mitten crabs below 3 mm CW did not show a reproductive response, in terms of gonad maturation, to either decreasing day length or temperature (Bauer and Tsukimura 22). It is possible that a minimum size requirement is a precondition for the reproductive cues mentioned above. If minimum size, day length, and temperature changes work in combination, a crab would need to be at minimum 3 mm CW shortly after the summer solstice in order to progress to reproductive maturity. Downstream migration of the adult crabs Large Chinese mitten crabs (4 7 mm CW) have been observed to congregate in the lower freshwater portions of San Francisco Estuary tributaries in the mid-to late-summer, which we describe as staging behavior (Rudnick 23). This staging behavior may be a sign of the beginning of downstream migration. Downstream-migrating adults are collected at water management facilities in the southern end of the Sacramento San Joaquin Delta in September and collections are sustained through October, with stragglers caught through January (Foss and Veldhuizen 21; Rudnick et al. 23). The crab has been suggested to migrate downstream very quickly; in Europe, downstream migration rates were estimated at 7 12 km/day, and as high as 18 km/day (Panning 1939a; Herborg et al. 23). It is unclear whether the cue for migration is tied to local changes such as precipitation or water temperature, or a more universal cue such as day length, or a combination of these factors. Increases in collection rates of downstream migrating adult mitten crabs in the San Francisco Estuary have been correlated with a decline in water temperature at the site of collection (Siegfried 1999). In a study of the Japanese mitten crab, Eriocheir japonicus, declining water temperatures correlated with the patterns of downstream migration of adult crabs (Kobayashi and Matsuura 199). In South San Francisco Bay, large numbers of crabs were observed to migrate in association with rain events (Culver and Walter 23). Mitten crabs migrate downstream as adults in the fall across all regions they occur, regardless of the fact that these regions exhibit a range of hydrologic patterns and climates in the fall (Table 3). Given the uniformity in timing among all populations of mitten crabs (native and introduced), a more universal environmental cue, such as photoperiod, may be the strongest influence on the timing of the downstream breeding migration. Adult crabs in their breeding grounds The location of mating for E. sinensis in Europe and China is suggested to be in saline water (Hoestlandt 1948; Zhao and Du 1988). Of female crabs collected from fresh water during their downstream migration to San Francisco Bay, none contained sperm in the sperm receptacles, suggesting that mating has not yet occurred (Bauer and Tsukimura 22). Although it has been suggested that attachment of eggs to pleopods requires a saline environment, above 2& (Panning 1939a; Ingle 1986), ovigerous females in the San Francisco Estuary have been collected primarily from San Pablo Bay and South San Francisco Bay, and to a lesser extent from Suisun Bay and Marsh, in salinities ranging between.1 and 3&, with a mean salinity at point of collection of 18& (Rudnick et al. 23). A wide range of sizes of reproductively mature adults has been reported throughout the world. Adult sizes reported from European populations range from 38 mm to more than 84 mm (Panning 1939a; Hoestlandt 1948; Ingle 1986) and sizes in Chinese populations of the crab have been reported from 38 to over 9 mm (Kobayashi and Matsuura 199; Jin et al. 1999; Zhang et al. 21). In a study of cultured Chinese mitten crabs in China, only a small subset were found to become reproductive at smaller sizes, in the range of 3 42 mm (Jin et al. 21;

14 346 Zhang et al. 21). In the San Francisco Estuary, reproductively mature mitten crabs collected from San Francisco Bay range between 3 and 9 mm carapace width, but the majority of adults collected have ranged in size from 4 to 7 mm (Rudnick et al. 23). The average size of reproductively mature mitten crabs in the North and South Bay populations has diverged over the period of the crab s establishment, so that average sizes of adult crabs collected from the South Bay (mean 4 mm CW) are significantly smaller than the average size of adult crabs collected from the North Bay (mean 6 mm CW) (Rudnick et al. 23). Although the reason for this size divergence is unclear, it is consistent with our discussion of growth rates and their variability with differing environmental conditions. Some of the tributaries to North San Francisco Bay are deeper than, and are cooler in fall and winter than, many South San Francisco Bay tributaries (Orsi 1999; Culver and Walter 22; USGS 23). It is possible that these habitat differences translate into a slower growth rate for North Bay crabs, so that they do not achieve the minimum size needed to commence maturation, and they therefore overwinter an additional year, leading to a larger size at maturity. Alternatively, the larger molt increment reported for North San Francisco Bay crabs relative to that of South San Francisco Bay crabs (see Age 1 section, above, and Time to Maturity Model, below), could influence the difference in size at sexual maturity. An increased understanding of the association between water temperature and growth rates of mitten crabs may help resolve this question. As discussed in the larval section, female E. sinensis may brood the egg cluster for 1 2 months, or egg development could be delayed until amenable environmental conditions exist. Given the timing of arrival of recently settled juveniles and the large range of sizes of age crabs found throughout the year in the freshwater tributaries of the San Francisco Estuary, it is likely that the hatching period is extended over several months. It has been suggested that adult mitten crabs have a single reproductive season and are short-lived after mating (Panning 1939a; Ingle 1986). In support of this hypothesis, we have never collected live adult male Chinese mitten crabs from San Francisco Bay later than May, with only a small number of adult females collected into the early summer (Rudnick et al. 23). Time to maturity model Rates of larval and megalopal development We chose to use Anger s (1991) rates of larval development for the model, as this data set is more comprehensive over multiple temperatures and salinities than our laboratory data. However, we documented longer development times found for Chinese mitten crab larvae raised from San Francisco Estuary crabs, suggesting that Anger s (1991) data could be conservative for time to metamorphosis (Table 2). During the time that the mitten crab has been present in the San Francisco Estuary, temperatures generally have ranged between and 2 C over the course of the year throughout the open waters of the Bay, and only reach temperatures as high as 23 C during a few weeks in summer in limited areas of the Bay (USGS 23); therefore, Anger s tested temperatures are relevant to the conditions likely encountered by mitten crab larvae in San Francisco Estuary. Megalopae raised from the San Francisco Estuary population of E. sinensis remained in this stage at a minimum of 21 days at 17 C and 2& in the laboratory, while Anger s data provides mean megalopal durations of 33 days at 12 C and 2 ppt, to 18 days at 18 C and 2 ppt. If these estimates of megalopal development time are added to zoeal development time, time to metamorphosis to the juvenile stage (time to completion of the larval and post-larval stages) ranges from about 4 to 93 days depending on temperature and salinity (Table 2). Juvenile growth rates Given the timing suggested for larval development and metamorphosis above, and using the estimated molting rate ((days to stage n+1) ¼ 8.83e.278 (days to stage n); Figure 3) and molt increments (22%; Figure 4) from laboratory studies described above, we constructed models of rates of growth over time for juveniles hatched in the early (December 1), mid-(march 1), and late (July 1) breeding season to the end

15 347 Carapace Width (mm) ºC larvae, 18% G.R. 12ºC larvae, 26% G.R. ºC larvae, 18% G.R. ºC larvae, 26% G.R. 18ºC larvae, 18% G.R. 18ºC larvae, 26% G.R. Age Age 1 Age 2 Dec Jun Dec Jun Dec Jun Dec Date Figure 7. Models of Chinese mitten crab growth rates based on December 1, March 1, and July 1 hatch dates, two temperatures during the period of larval development, and two rates of incremental growth (G.R.). Lower temperatures of larval development (12 and C, see Table 2) are used for December and March hatch dates, as these temperatures are characteristic of the range of temperatures in San Francisco Bay likely encountered by mitten crab larvae in winter and early spring; while higher temperatures ( and 18 C) are used for temperatures during development of larvae hatched in early summer. of their first year of growth (Figure 7). We used rates of larval development associated with temperatures of 12 and C for larvae hatching in early- and mid-breeding season, and rates associated with and 18 C for larvae hatching in the late-breeding season, as these temperatures are similar to temperature increases in San Francisco Estuary over the course of the breeding season. Models suggest that crabs hatched early in the season could reach sizes close to 3 mm CW by the end of their first year of growth, while crabs hatched late in the season may achieve less than half this size in their first year (Figure 7). This model can inform year class assignments for young juvenile crabs collected from Coyote Creek (Figure 2): based on model estimates, < mm carapace width crabs collected in April from Coyote Creek are age crabs hatched in late winter or early spring. Crabs > mm CW collected early in the sampling period are likely crabs hatched the previous year. Crabs between mm CW could be age crabs hatched early in the reproductive season or age 1 hatched late in the reproductive season of the previous year. Although our model predicts crabs will be larger than mm at age 1, if slower fall and winter growth rates are factored into the model, it is possible that some crabs may be smaller than mm at age 1. To estimate growth rates of age 1 crabs, the average growth increments of 18 and 26% from South Bay and Delta field data (Age 1 crabs section) were added to the model. These estimated values were combined with growth rates at various temperatures of crabs born throughout the reproductive season of the previous year. Crabs hatched early the previous year (December hatch) can, in this model, achieve sizes between 33 and mm CW by the end of the age 1 calendar year, while age 1 crabs hatched late in the previous year s reproductive season (July hatch) achieve sizes between 28 and 38 mm CW by the end of age 1 (Figure 7). This growth rate model suggests that San Francisco Estuary crabs could reach sizes between 39 and 78 mm CW by the end of age 2 (Figure 7). These sizes overlap with the range of sizes of adult mitten crabs in San Francisco Bay (see Adults section above). The divergence in sizes modeled by incorporating two incremental growth rates also matches the pattern of size divergence we have seen in northern and southern San Francisco Estuary populations of the crabs. For all crabs, however, if longer intermolt periods or smaller growth increments associated with lower temperatures are incorporated into the calculation of rate of growth, crabs at the end of age 2 will be smaller than the estimates in this model. If a decrease in growth rate during the cold season is incorporated into the model, some crabs might not reach reproductive size at Age 2, and may need to overwinter past age 2 to attain a minimum reproductive size. While this model incorporates variability in growth increment (18 and 26%), and the exponential equation for juvenile growth rates incorporates a slowing in molting rate over time, the model does not account for seasonal variability in the intermolt period. Given that growth may slow, if not cease, during the cooler winter and early spring months, this model may overestimate growth rates. The model also does not account for the fact that warm temperatures during summer months could, conversely, lead to a shortening of the intermolt period. The sizes we present in our model, therefore, should be seen as broad estimates likely to be strongly influenced by seasonal temperature changes.