A life history model for the San Francisco Estuary population of the

Chinese mitten crab, Eriocheir sinensis (Decapoda: Grapsoidea)

Deborah Rudnick1,7, Tanya Veldhuizen2, Richard Tullis3, Carolyn Culver4, KathrynHieb5 & Brian Tsukimura6,*1University of California, Berkeley, California, USA; 2California Department of Water Resources,Sacramento, California, USA; 3California State University, Hayward, California, USA; 4University ofCalifornia at Santa Barbara, California, USA; 5California Department of Fish and Game, Stockton,California, USA; 6Department of Biology, California State University (CSU), Fresno, California, USA;7Present address: 10,000 Years Institute, Bainbridge Island, Washington, USA; *Author for correspondence(e-mail: briant@csufresno.edu; fax: +1-559-278-3963)

Received 24 July 2003; accepted in revised form 15 June 2004

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 becomeestablished over hundreds of km2 of the San Francisco Estuary. Ecological and economic impacts of thisinvasive species motivated our search for a greater understanding of the crab’s life history as an impor-tant 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 theydevelop into adults. Environmental signals may stimulate gonad development that is followed by adownstream migration beginning at the end of summer. Mating occurs after the crabs reach salinewater. 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 aminimum of 2 years in low salinity or freshwater habitat, and predicts that most California mitten crabsare at least 3 years old before becoming sexually mature. Environmental factors strongly influence thetiming and duration of the crab’s life stages, and are discussed in the context of a gradient of develop-ment times for worldwide populations of this important invasive species.

Introduction

The Chinese mitten crab, Eriocheir sinensis(Decapoda: Grapsoidea), was first detected inSan Francisco Estuary in 1992. A populationexplosion of mitten crabs occurred in the Estuaryin 1998, prompting widespread concern aboutthis species’ potential impacts. Native to riversand estuaries of the west coast of North Koreasouth to Shanghai, China, invasive populationsof E. sinensis also exist throughout freshwaterand estuarine systems of central and westernEurope as a result of introductions over the past

century (Hoestlandt 1948; Haahtela 1963; Ingle1986; Ja _zd _zewski and Konopacka 1993; Dhurand Massard 1995; Clark et al. 1998; Cabral andCosta 1999; Gollasch 1999).

Introduced populations of the Chinese mittencrab have caused several economic and ecologicalimpacts. Commercial and recreational fishingoperations have been hindered by bait stealingand damage to gear and the catch by the crab(Panning 1939a; Rudnick and Resh 2002). InCalifornia, the mitten crab has also interferedwith operations at federal and state water diver-sion plants and power plants (Siegfried 1999;

Biological Invasions (2005) 7: 333–350 � Springer 2005

Veldhuizen and Stanish 1999). The burrowinghabit of E. sinensis has undermined the integrityof stream banks and levees throughout its intro-duced range (Peters and Panning 1933; Duttonand Conroy 1998), particularly in south SanFrancisco Estuary watersheds (Rudnick et al.2003). The mitten crab likely impacts freshwaterand estuarine food webs at many levels, as it hasan opportunistic diet that includes algae, detritus,and a variety of benthic macroinvertebrates (Pan-ning 1939a; Hoestlandt 1948; Gollasch 1999;Rudnick and Resh in review). These impactshave been, and likely will continue to be, exacer-bated by population explosions such as was seenin 1998 in San Francisco Estuary; similar rapidfluctuations in abundance have been reportedfrom several European countries (Panning 1939a;Gollasch 1999; Herborg et al. 2003).

Research conducted on populations of the mit-ten crab underscores the spatial and temporal vari-ability of this species’ life history across its globaldistribution. For example, E. sinensis are reportedto take 3–5 years to reach sexual maturity innorthern Europe (Panning 1939a; Gollasch 1999),while 1–2 years to maturity has been reported forsouthern and central China (Hymanson et al.1999; Zhang et al. 2001). There are substantial dif-ferences in crab abundance among populationsthroughout the world; for example, periodicallymassive abundances are found in Germany andEngland (Clark et al. 1998; Gollasch 1999), whilerelatively small populations have persisted in sev-eral countries such as Finland and Poland (Haah-tela 1963; Ja _zd_zewski and Konopacka 1993).

Efforts to understand the ecology of the mittencrab and control its impacts in California havebeen hindered by an incomplete understanding ofthe population dynamics of this species.Increased understanding of the factors that drivemitten crab abundance and distribution couldhelp scientists and managers better predict andprepare for years with high abundance. Forexample, the 1998 mitten crab population explo-sion lead to near-total mortality of fish andgreatly increased handling and engineering costsat the US Bureau of Reclamation pumping facil-ity and fish bypass tanks in tributaries to SanFrancisco Estuary (Siegfried 1999). Improvingpredictive power for the population dynamics ofthis species could help better prepare for years ofhigh crab abundance and reduce impacts on

wildlife and water supply. A greater understand-ing of the factors that control abundance anddistribution can also inform our understandingof the preferred habitats and geographic limits ofdistribution of this species, improving risk assess-ment for future invasions of the crab.

Using the scientific literature available for thisspecies and data we have collected, we present adiscussion of the life history of the San FranciscoEstuary population of the Chinese mitten crab.The model is organized into four developmentalstages (larva, megalopa, juvenile, and adult), withdiscussions of the physiological and ecologicalrequirements and preferences that characterizeeach stage. We supplement our data for the SanFrancisco Estuary population of the crab(Table 1) with published data from native andintroduced populations, and examine similaritiesand differences across these data sets, discussingenvironmental factors that may shape these dif-ferences. Our discussion is focused primarily onthe seasonal timing and distributional patterns ofthe four life stages of the crab as a foundationfor building the life history model.

After the life stages are discussed, we describea model based on data about larval developmentand juvenile growth rates to estimate time to sex-ual maturity for the San Francisco Estuary popu-lation of the mitten crab. Our discussion andmodel identifies factors that may assist in predict-ing the population dynamics of the mitten crab,and outlines areas that warrant additionalresearch to solidify our understanding of mittencrab life history.

Study system

The San Francisco Estuary (N 37�45¢, W 122�26¢),which includes South San Francisco Bay, centralSan Francisco Bay, San Pablo Bay (we refer tothe latter two areas collectively as ‘North SanFrancisco Bay’), Suisun Bay and Marsh, and theSacramento–San Joaquin Delta (the Delta),forms the largest estuary (approximately1600 mi2) on the west coast of North America,draining about 40% (153,000 km2; 40 millionacres) of California’s surface area (Nichols et al.1986; Hymanson et al. 1994) (Figure 1). TheEstuary is a large, tidal, and highly modified eco-system (Nichols et al. 1986). About 90% of theEstuary’s freshwater inflow originates from the

334

Delta watershed (SFEP 1992). The region ischaracterized as having a Mediterranean climatewith cool, wet winters (November–April) andwarm, dry summers (May–October) (SFEP1992). On average, Estuary temperatures rangefrom about 10 �C in winter to 20 �C in summer(Herrgesell et al. 1983; USGS 2003).

The Chinese mitten crab encounters a mosaicof physical and chemical conditions throughoutthe San Francisco Estuary. South San FranciscoBay is a large (554 km2), shallow bay with anaverage depth of 3 m and silt and clay sediments(SFEP 1992). Salinities in the South Bay rangefrom 30& in the Bay to approximately 15& attributary mouths. South Bay water temperaturesrange between about 10 �C in winter to 23 �C insummer, and are often slightly (1–3�) warmerthan temperatures in the central and north bays(USGS 2003). Tidal influence extends 5–8 km uptributaries (Rudnick et al. 2003) that are shallow,short (<50 km), and drain small steep watershedswith very short lag times and high peak runoffs.To the north, San Pablo Bay is a large(272 km2), shallow bay characterized by expan-sive tidal mudflats. To the east of San PabloBay, salinities in the dredged channels and shoalsof Suisun Bay are highly variable in response tochanges in freshwater outflow from the Sacra-mento-San Joaquin Delta (Herrgesell et al. 1983),and range from approx. 0.2 to 10.6& (Hyman-son et al. 1994). The tidal and freshwater habi-tats of the Sacramento–San Joaquin Delta(2978 km2) is the confluence of several major riv-ers; depths range from <1 to 5 m in shallowopen water to >15 m in channels, and annualmean salinities range from 0.06 to 2.27& (Hy-manson et al. 1994). Water temperatures in theDelta range between about 10 �C in winter to20 �C in summer (Herrgesell et al. 1983), butsome regions of the Delta can reach 25 �C duringsummer months (DWR 2001).

Materials and methods

Data supplying the model and life historydiscussion

Information used to generate the life historymodel includes data published about native andintroduced populations of the mitten crab, andT

able

1.California

data

sets

contributingto

thedevelopmentoftheChinesemittencrablife

history

model.

Crablife

stage

Typeofdata

Researchlocation

Primary

researcher

Institution

Periodof

data

collection

Reference

(ifpreviously

published

data)

Larvae

Growth

rates

Laboratory

R.Tullis

California

State

University

Hayward

2001–2002

Juveniles

Growth

rates

Laboratory

R.Tullis

California

State

University

Hayward

2001–2002

Growth

rates

SanFranciscoBayand

Sacramento/SanJoaquin

Delta

T.Veldhuizen

California

DepartmentofWater

Resources

1999–2001

Abundance

and

size

distribution

South

SanFranciscoBay

C.Culver

University

ofCalifornia

Santa

Barbara

2001

Culver

andWalter

(2002)

Growth

ratesand

size

distribution

South

SanFranciscoBay

D.Rudnick

University

ofCalifornia

Berkeley

2000–2001

Adults

Reproductive

development

Laboratory

B.Tsukim

ura

California

State

University

Fresno

2000–2003

Toste(2001),

Bauer

and

Tsukim

ura

(2002)

Adultabundance

andmorphology

SanFranciscoBayand

Sacramento/SanJoaquin

Delta

K.

Hieb

and

S.

Foss

California

DepartmentofFish

andGame/DepartmentofWater

Resources/U

SBureauofReclamation

1996–2003

Rudnicket

al.(2003)

335

published and unpublished data from theauthors’ research (Table 1). Here, we describemethods for research that has not previouslybeen published and was used to develop the lifehistory model: (1) larval and juvenile growthrates of mitten crabs raised in the laboratory; (2)juvenile crab recruitment patterns documented ina South Bay tributary; and (3) incrementalgrowth rates of juveniles in the field.

Larval and juvenile growth ratesMitten crab eggs were harvested from six gravidfemales collected from the Delta and bred in thelaboratory at California State University, Hay-ward. Upon hatching, all eggs were combined.The resulting larva were maintained in fingerbowls containing 20–30 individuals kept at 20&at 17 �C and fed Artemia nauplii. The juveniles

were maintained as individuals in individual fin-ger bowls with the same water conditions andfed salmon pellets (Nelson & Sons suppliers) andEgeria densa, an aquatic macrophyte. Carapacewidth (CW) of juvenile mitten crabs was mea-sured within a few hours following each moltusing Vernier calipers at the widest part of thecarapace between the fourth anterolateral teeth.Time until the first member of the group transi-tioned to the subsequent stage or molt (minimumtime to stage) was recorded for Zoea II, II, andV, the megalopa, and the first 14 juvenile molts.

Juvenile crab recruitment and size patternsIn order to collect data on abundance and sizesof newly settled mitten crabs, recruitment collec-tors were placed in the high tidal portion (£5&salinity) of Coyote Creek, Santa Clara County,CA (Figure 1). Three sets of collectors weredeployed at the site in mid-January because itwas unlikely that mitten crab larvae would bepresent earlier in the season (see life history dis-cussion below), and were removed mid-Augustwhen settlement of decapods had not beendetected for two consecutive months. Each set ofcollectors consisted of four dish scrub pads (Tu-ffy�) attached to a weighted polypropylene lineapproximately 1 m from the bottom of the line.Collectors were retrieved and replaced 2· permonth. Retrieved collectors were placed in plasticbags and frozen until processing. Samples werethawed in the laboratory and examined under amicroscope for crab megalopae and juveniles. Allcrabs were identified to species and enumerated.Carapace width (CW) of mitten crabs was mea-sured either microscopically (crabs <5 mm) orusing Vernier calipers (crabs >5 mm).

Juvenile mitten crabs were also collected in theupper tidal portion of Calabazas Creek, a tribu-tary to South San Francisco Bay, by D. Rudnickusing artificial shelter traps with a set time ofapproximately 2 weeks, between November 2000and October 2001 (Rudnick 2003; Veldhuizen2003). This passive trap is composed of multiplestacked tubes (6 in. diameter) that are used asshelter by the juvenile crabs. This substrate offerslarger refugia than the Tuffy collectors describedabove, and a range of larger crabs was corre-spondingly collected in these tube traps. Col-lected crabs were measured (CW) and sexed (can

Figure 1. Distribution of the Chinese mitten crab, in bold

black, in the San Francisco Estuary in 2001. Reports and

sightings of the crabs from individuals and monitoring pro-

grams 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.

336

be determined for crabs >7 mm CW (Rudnick2003)).

Incremental growth rates of juvenile crabsMitten crabs were collected in Calabazas Creek, atributary to South San Francisco Bay, and in low-salinity tributaries to the Sacramento–San JoaquinDelta (Figure 1) using artificial shelter traps with aset time of approximately 2 weeks, as describedabove. Molts were assumed to belong to crabscaptured in the same trap when those crabs weresoft-shelled or appeared to have recently molted(light-colored setae on chelae, no epiphyticgrowth), were slightly larger in size (within 10 mmcarapace width (CW)), and of the same sex. CW ofcrabs and molts was taken between the fourthanterolateral teeth using Vernier calipers. Tenpairs of recently molted crabs (20–40 mm CW)and their molts were collected in Calabazas Creek,South San Francisco Bay, between November2000 and October 2001. Six recently molted crabs(19–49 mm CW) and molts were collected in theDelta from August 2000 to July 2001. Linearregression was used to determine the relationshipbetween pre- and post-molt sizes. Because of thesesmall sample sizes, we did not test for significantdifferences between the molting rates from thesetwo data sets, but rather used the resulting rangeof values as a way of adding a measure of variabil-ity to our model.

Development of time-to-maturity estimates

We developed a model of the time span for mit-ten crabs to reach sexual maturity from hatching.To construct the model, we used informationabout larval development rates with growth ratedata for juvenile mitten crabs. To incorporateinformation about growth rate variability, weused multiple growth rates under varying temper-atures, salinities, and habitats from our field andlaboratory studies. Estimates of time to maturityare a function of:(1) Timing of larval hatching. We used three

hatching times: December 1, March 1, andJuly 1, as these times cover the range of theestimated mitten crab breeding period.

(2) Rates of larval development under varyingtemperatures. We used Anger’s (1991) larvaldevelopment rates, because these rates wererelatively consistent with our laboratory data,

and provided more information about devel-opment rates under multiple temperatures andsalinities. We used lower water temperatures,of 12 and 15 �C, to guide time of developmentfor early- and mid-season hatched larvae, asthese temperatures are appropriate to Bayconditions during the winter and spring, whilehigher temperatures (15–18 �C) were used forlate-hatching larvae that develop in the war-mer spring and summer temperatures of SanFrancisco Bay (USGS 2003).

(3) Molting rates for young juvenile mitten crabsraised in the laboratory. A function describingthe time between molts was generated from thegrowth rate curve developed from this data.

(4) Incremental growth rate, or the increase ofbody size during a single molt. These data werederived from crabs raised in the laboratory fornewly settled juvenile crabs, and for largercrabs (‡ 20 mm CW) collected in the field inSouth San Francisco Bay and in the Delta.

Larval development rates were generated bystarting with one of the three hatching dates,then adding time to metamorphosis based ontemperature. The rate of growth of the first yearjuvenile was modeled by starting with a 2 mmCW (newly settled juvenile as determined fromlaboratory studies and confirmed by field data)crab and, using our data for the frequency ofmolting and growth increments of young crabs,generating estimates of the amount of growth ajuvenile could achieve in its first year of life.Rates of incremental growth generated from twosets of field data for older juvenile crabs wereused to estimate rates of growth for crabs largerthan 20 mm CW. By combining the data for timefrom hatching to metamorphosis with growthrate data through the first year and up to sizesconsistent with sizes of sexually mature crabs col-lected from San Francisco Bay, we establishedestimates for total time for mitten crabs to reachmaturity from hatching.

Results and discussion

Life history of the Chinese mitten crab

LarvaeThere have been few collections of mitten crablarvae from the San Francisco Estuary; therefore,

337

hatching is inferred from the timing of the pres-ence of ovigerous females. The majority of ovig-erous female Chinese mitten crabs occur betweenNovember and March in the open waters of theSan Francisco Estuary, with smaller numbers ofovigerous females collected from April to June(Rudnick et al. 2003). Female mitten crabs haveextruded multiple broods in the laboratory; how-ever, subsequent broods contained lower num-bers of viable eggs (C. Culver and R. Tullis,unpublished data). Under laboratory conditionsin California, eggs of E. sinensis hatched inapproximately 30 days at 17 �C and 20& salin-ity, but have been reported to take longer (ordeveloping more slowly) at lower temperatures inother laboratory experiments (Anger 1991)(Table 2).

In the cold waters of northern Europe, embry-onic development may be slowed, so that femaleshold on to fertilized eggs through the winter,moving to shallower, warmer waters in thespring, where the larvae are released (Ingle 1986).Among other decapod crustacea, there is alsoevidence for delays in development and mainte-nance of eggs until favorable conditions com-mence for hatching (Sastry 1983; Adiyodi 1985).It is unknown if delays in egg development andhatching occur for the San Francisco Estuarypopulation of the crab. If development is notdelayed for ovigerous females early in the repro-ductive season, eggs could feasibly hatch as earlyas the beginning of December. Overall, the per-iod of egg production and development in theSan Francisco Estuary spans November to June(Table 3).

Mitten crab eggs hatch into free-swimmingpelagic larvae. E. sinensis typically has five larvalstages (Zoeae I–V) (Kim and Hwang 1994;Montu et al. 1996). Mitten crab larvae are eury-haline; however, they still require at least 16–17& salinity to survive in the intermediate zoealstages in the laboratory (Anger 1991). Zoeae Ihave a larger capacity to tolerate lower salinitiesthan intermediate stages (Anger 1991; R. Tullis,pers. obs.). These changes in salinity preferencessupport a mitten crab larval association with thebrackish water of estuaries at hatching, followedby transport of the larvae away from shore bycurrents to higher salinity waters during later lar-val stages (Anger 1991). This pattern of move-ment has been reported for other brachyuran

crustacean larvae that are exported to the coastalocean (Garvine et al. 1997; Epifanio and Garvine2001). However, it is unknown whether mittencrab larvae undergo coastal export, or if a larvalretention mechanism might help them remain inthe estuary.

Water temperature likely influences both sur-vival and rate of development of mitten crab lar-vae. Anger’s (1991) laboratory data indicatedthat higher salinities and temperatures were cor-related with faster rates of development, withtime to megalopal stage ranging between 18 and74 days (Table 2). Mitten crabs raised in aqua-culture conditions in China at 23 �C passedthrough each zoeal stage in 2–4 days, completinglarval development in about 15 days (Zhao1988). Our data suggest a longer time to develop-ment than found in Anger’s data (Table 2); partof this variation may be due to the fact that weused slightly lower salinities than those used byAnger, who detected slightly faster developmentrates in early larval stages with higher salinities(25&) (1991). Temperatures below 9 �C werelethal to larvae in German laboratory experi-ments (Anger 1991), yet the crab’s distribution inNorthern Europe includes waters that are regu-larly colder than this temperature (Anger 1991).Thus, the lethal limit may be lower in naturethan has been indicated by laboratory studies.

MegalopaeThe megalopa is the post-larval stage that occursprior to settling of the crab as a benthic juvenile.Mitten crab megalopae have been suggested touse tidal currents to move into river systemsfrom the estuary (Panning 1939b). Active migra-tion towards less saline waters has beendescribed for other megalopae in the grapsoidsuperfamily to which mitten crabs belong (Ryanand Choy 1990). In the laboratory, megalopaeshow signs of increased tolerance to low salinities(Anger 1991), and those raised in the laboratoryin California tolerated fresh to low salinity waterof 0–5& (R. Tullis, pers.obs.). In natural habi-tats, megalopae have been collected in low salin-ity (0–5&) areas throughout the world(Schnakenbeck 1933 as cited in Anger 1991; Pan-ning 1939a; Ingle 1986; Jiang Dinhe, pers.comm., Culver and Walter 2002). Thus, ashypothesized by Panning (1939a) and Anger(1991), the megalopal stage is likely responsible

338

Table

2.Ratesoflarvalandpost-larvaldevelopmentasafunctionofsalinityandtemperature.

Larvalstage

R.Tullisdata

Anger

(1991)

Minim

um

number

ofdaysto

stage

at17

�C,20

pptsalinity

Salinityaat

12

�Cb:optimalc

(totalrange

withstood)

Daysat

12

�Cand25ppt:

meanvalued

Salinityat

15

�C:optimal

(totalrange

withstood)

Daysat

15

�Cand

25ppt:mean

value

Salinityat

18

�C:optimal

(totalrange

withstood)

Daysat

18

�Cand

25ppt:meanvalue

Zoea

In.d.

25

11

20–32

715–32

5

(15–32)

(10–32)

(10–32)

Zoea

IIn.d.

25

10

25

615–32

5

(15–32)

(15–32)

(10–32)

Zoea

III

57

25

10

25

715–32

4

(15–32)

(15–32)

(15–32)

Zoea

IV72

25

12

25

820–32

5

(15–32)

(15–32)

(15–32)

Zoea

Vn.d.

25

17

25

11

32

8

(20–32)

(20–32)

(15–32)

Tim

eto

megalopa

78

60

39

27

Megalopa

21

None

33

25

23

(25–32)

18

(20–25)

(25–32)

20–32

Totaldaysto

metamorphosis

99

93

62

45

First

columnisourdata

(R.Tullis);remainingcolumnsare

data

summarizedfrom

Anger

1991.

aSalinitiestested

byAnger

were10–32&

in5&

increm

ents.

bTem

peraturestested

were6,9,12,15and18

�C;temperaturesof6and9

�Cdid

notallow

forsurvivalbeyondZoea

I.cOptimalconditionsare

those

withthehighestpercentsurvivalobtained

amongthesalinitiestested

atthegiven

temperature.ForZoeaeI–IV

,thehighestsurvivalrateswere

>60%

atthesalinityshown;forZoea

5,>50%,andforMegalopa,>

40%

(Anger

1991).

dConfidence

intervalscould

notbetranslatedfrom

graphic

data;in

general,confidence

intervalsforthesevalues

ranged

from

±0.1

to±

0.5

days.

339

Table

3.Comparisonsofselect

aspects

ofthetimingandconditionsofthelife

history

oftheChinesemittencrabin

itsnativeandintroducedranges.

Region

Extentof

range

First

record

ofspecies

General

estuarine

temperatures

(winter–

summer)

Periodof

larval

settlement

Sizeofsexually

mature

adults

Collected

(mm

CW)

Periodof

downstream

migration

Breeding

periodc:range

(peakifknown)

Years

of

population

peak

abundance

Suggested

life

span

Chinaa

24–42�N

Native

8–27

�C(Y

angtze)

April–June

38–90

(aquaculture:

someas

smallas30)

August–

Novem

ber

(September)

October

to

April

(Decem

ber)

n.d.;low

since

1960s

1–3years

W.Europeb

Germany

52–54�N

1912

6–21

�CMay–August

38–84

August–

October

October–May

1930–39;

53–60;

69–75;79–83;

93–99

4–6years

France

45.5–49.5

�N

1930

8–23

�CApril–July

50–90

August–

October

n.d.

1940s(no.

France),

Late

1950s(so.

France)

n.d.

England

(Thames)

51.5

�N

1936

5–23

�Cn.d.

n.d.

n.d.

n.d.

Early1990s

n.d.

California

37–40�N

1992

8–25

�CApril–June+

?30–95

August–

Decem

ber

Novem

ber–

June

(Decem

ber–

February)

1997–1999

2–4years;aver-

agemaybe3

Data

sources

Cohen

and

Weinstein

(2001),

Hymanson

etal.(1999)

Panning(1939),

Hoestlandt

(1948),Herborg

etal.(2003)

Cohen

and

Weinstein

(2001),

USGS(2003)

Panning(1939),

Hymanson

etal.(1999),

thispaper

Hoestlandt

(1948),Jinet

al.

(1999);Zhang

etal.(2001),

Rudnicket

al.

(2003)

Hymanson

etal.(1999),

Gollasch

(1999),

Hoestlandt

(1948),Rudnick

etal.(2003),

Herborg

etal.

(2003)

Panning

(1939a,b),

Hymanson

etal.(1999),

Rudnick

etal.(2003)

Gollasch

(1999),

Cohen

and

Weinstein

(2001),Rudnick

etal.

(2003),

thispaper

Panning

(1939a,b),

Hymanson

etal.(1999),

thispaper

aData

forwildpopulationscomes

primarily

from

theYangtzeRiver

(28–32

�N);

additionaldata

asnotedfrom

aquaculturedmittencrabpopulationsraised

primarily

in

ponded

conditions).

bRangeofthemittencrabincludes

severalother

Europeancountries,

includingPoland,TheNetherlands,

Czechoslovakia

Portugal,andSpain

(See

Rudnicket

al.2003);the

threecountrieschosenare

those

forwhichsubstantiallife

history

data

wasfound.

cBreedingperiodincludes

matingandtheperiodin

whicheggsare

carriedbythefemale

untilhatching.

340

for movement towards lower salinity water inpreparation for metamorphosis into a benthicjuvenile.

Movement towards low salinity habitat duringthe pelagic stage of this organism may be affectedby outflow during the period of migration. Littleis known about the effects of increased freshwa-ter outflow on the retention of zooplankton(Kimmerer et al. 2002). If megalopae have someability to cue towards freshwater sources, higherflows may attract more crabs, leading to a posi-tive correlation between settling and discharge.However, high flows could also delay or reducesuccess of upstream migration of these very smallorganisms by preventing megalopae and youngbenthic crabs from reaching the habitat requiredfor their development. One finding that supportsthe latter hypothesis is that the only collectionsof megalopae (n ¼ 3) in South San FranciscoBay occurred in April simultaneously with a sub-stantial decline in water discharge that had notbeen seen since January of that year (Culver andWalter 2002). Studies of an invasive populationof the Chinese mitten crab in the UK suggested acorrelation between long-term declines in dis-charge from freshwater systems with increasedabundance of this species (Atrill and Thomas1996). However, as water temperature and salin-ity are also affected by flow, additional informa-tion is needed to decipher the potential influenceof these factors on mitten crab settlement.

There has been minimal research conductedexamining the timing or location of San Fran-cisco Estuary mitten crab megalopae. One mittencrab megalopa was collected in North San Fran-

cisco Bay as early as February (K. Hieb, pers.obs.) and a few were collected in April in twotributaries of South San Francisco Bay (Culverand Walter 2002). As larvae likely hatch as lateas early summer (see larval section above), mittencrab megalopae probably occur into the summer.Panning (1939a) reported that in Germany,where winter and spring conditions are muchcooler and wetter than California, megalopae set-tle in July/August in warmer years, but not untilOctober during cooler/wetter years.

JuvenilesAge 0 crabs. Age 0 crabs are defined for the pur-pose of this life history model as juvenilesbetween their date of metamorphosis and thestart of the following calendar year. Age 0 crabsbegin as the initial crab-like form that followsfrom the pelagic megalopa. The newly settledjuvenile crab is benthic and initially resides inwater between 1 and 20& salinity (Culver andWalter 2002; Rudnick et al. 2003). The carapacewidth (CW) of newly metamorphosed juvenilesraised in the laboratory from San FranciscoEstuary larvae is 2–3 mm, similar to sizesreported for newly settled mitten crabs in othercountries (Panning 1939a; Montu et al. 1996).These recently settled juveniles were collectedover a large temporal distribution (April–June) ina South San Francisco Bay tributary (Figure 2).

Young mitten crabs molt frequently, approxi-mately every 2 weeks for the first 8–10 molts inthe laboratory at 17 �C (Figure 3). Similar toother brachyuran crustacea (Hartnoll 1982), therate of molting decreases as mitten crabs grow

0

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1/29/2001 2/28/2001 3/30/2001 4/29/2001 5/29/2001 6/28/2001 7/28/2001 8/27/2001

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er o

f cr

abs

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Figure 2. Number of juvenile mitten crabs of three size classes collected biweekly between January and August 2001 on Coyote

Creek, a tributary to South San Francisco Bay. Data provided by C. Culver.

341

larger (Figure 3; Zhang et al. 2001). The incre-mental growth rate of San Francisco Estuaryjuvenile mitten crabs raised in the laboratory aver-aged 22% CW increase per molt (Figure 4). Thedistribution of sizes of early staged crabs fromnatural habitats supports the occurrence of a moltincrement around 22% in South Bay tributaries(C. Culver, unpublished data), and is similar toincrements reported for small crabs in Germany(24%) (Panning 1939a).This molt increment issimilar to growth rates reported for other youngjuvenile grapsoid crabs (Spivak 1988; Luppi et al.2002) and other decapods (Hartnoll 1982).

The growth rate of the young juvenile mittencrab likely has a direct relationship to water tem-perature, with colder temperatures lengtheningthe intermolt period, as has been reported forother brachyuran crustacea (Hartnoll 1982). Mini-

mal growth was reported for a Chinese popula-tion of Chinese mitten crabs between Januaryand July, with molting rates increasing duringthe warm summer months (Jin et al. 2001). Astemperatures in freshwater tributaries to SanFrancisco Bay drop in the autumn, mitten crabsmay slow or cease growing in the winter.

It has been suggested that mitten crabs remainin brackish habitats through their first winter,and do not commence migration into fresh wateruntil the following year (Panning 1939a). In Cali-fornia, young juveniles (<10 mm) are found intidally influenced, low salinity (1–10%) habitats(Culver and Walter 2002; Rudnick et al. 2003).On a few occasions, small crabs (<7 mm CW)have been collected in fresh water in the easternSacramento–San Joaquin Delta, 45–65 kmupstream of North San Francisco Bay (Veldhui-

days to molt N+1 = 8.5834e0.2782(days to molt N)

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om

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rt o

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ven

ile l

ife

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e

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.

150 crabs) molted to the next stage. Data provided by R. Tullis.

new CW = 1.2248 (old CW)R2 = 0.8997

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Figure 4. Relationship of pre- and post-molt sizes (carapace width) of juvenile mitten crabs. (a) (n ¼ 10) 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.

342

zen 2003). For the most part, however, juvenilessmaller than 10 mm CW are not found in fresh-water 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 veryearly in the previous reproductive season). By thistime, the crab is readily identified as male orfemale, as their abdominal shape is clearly differen-tiated (D. Rudnick, T. Veldhuizen, pers. obs.). Inboth sexes the setae on the chelae, from which thecommon name ‘mitten crab’ derives, are evident.

Our field studies documented molt incrementsof approximately 18% in crabs between 20 and40 mm collected from tributaries to South SanFrancisco Bay (Figure 5a), and about 26%among similarly sized crabs collected from the

Sacramento/San Joaquin Delta (Figure 5b). Stud-ies of Chinese populations of the mitten crabhave reported the increase in carapace width permolt (the growth increment) between 13 and 26%for crabs between 21 and 63 mm CW (Kamps1939 as cited in Zhang 2001).

Juvenile mitten crabs begin their movementinto freshwater habitat at a size consistent withmodel estimates for the crabs at the beginning ofage 1 (approx. 15–30 mm CW, see time to matu-rity model below). This upstream migration maybe rapid (1–3 km/day) (Panning 1939a). Little isknown about the cues that initiate this migration.Environmental cues may include temperature orincreasing day length (following the winter sol-stice). Upstream migration could be triggered byincreases in water flow (Gollasch 1999). Othershave suggested that crab density and food qual-ity/quantity may influence upstream migration ofjuvenile crabs, such that no upstream migrationoccurs if crab densities are low and food avail-ability is high (Panning 1939a; Ingle 1986). Sam-pling in tidally influenced (1–10&) South Baytributaries has procured some large (40 mm plus)crabs throughout the summer and fall that maybe older crabs that never left this habitat(Figure 6).

In California, actively upstream-migrating crabswere collected in the tributaries upstream of theDelta from mid-January through mid-Marchduring the population boom in 1998 (K. Hieb,pers. obs.). Small (approximately 20 mm CW)crabs and molts have been collected in South SanFrancisco Bay tributaries at least 10 kmupstream from of the Bay in May and June(Rudnick 2003), suggesting that age 1 crabs moveinto freshwater habitat by late spring.

Age 2+ crabs. Our size models estimate that mit-ten crabs range in size from 25–49 mm CW atthe beginning of age 2 (see time to maturitymodel below). Crabs in this size range collectedfrom both North and South Bay watersheds arecharacterized by several morphological changesassociated with progression to sexual maturity,including: increased growth of setae on the walk-ing legs, increase in fullness of the mittens ofsetae on the front claws, particularly in males; infemales, setae begin to form around the outeredge of the abdomen and the abdomen becomesmore rounded and fills in a larger portion of the

new CW = 1.1829 (old CW)

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m)

(a)

(b)

Figure 5. Relationship of pre- and post-molt sizes (carapace

width) of juvenile mitten crabs. (a) (n=10) collected from

Calabazas Creek, South San Francisco Bay. (b) (n ¼ 6) col-

lected 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 popula-

tion of mitten crabs.

343

underside of the carapace; and in males, thesperm ducts become fully developed and clearlyvisible when the abdomen is lifted away from thecarapace (Hoestlandt 1948; Rudnick 2003).

Little is known about the growth rate of age 2mitten crabs in California. It has been suggestedthat the intermolt period increases and growthincrement decreases as the crab ages; in Ger-many, incremental growth rates of small juvenilesaveraged 24%, but crabs ‡70 mm in carapacelength (similar to CW) had a molt increment ofonly 11% (Panning 1939a; size of the ‘smallerjuveniles’ 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 5 times during their second

year, and 2 to 3 times during their third… theolder crabs shed only once a year’’ (pp. 370–371). Decreased molt increments and increasedmolt intermolt periods typically occur withincreasing size of decapod crustaceans (e.g.,Hartnoll 1982; Seiple and Salmon 1987; Luppiet al. 2002).

AdultsBefore downstream migration to the breedingground commences, mitten crabs’ gonads beginto develop. Females raised in ponds in Chinahave been shown to undergo ovarian develop-ment prior to migration (Zhang et al. 2001), anddissections of female mitten crabs collected fromfreshwater tributaries to the San Francisco Estu-

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Figure 6. Histograms of carapace widths of Chinese mitten crabs collected by passive traps between December 2000 and August

2001 in Calabazas Creek, a tributary to South San Francisco Bay. Storm events precluded sampling in January–March. Data pro-

vided by D. Rudnick.

344

ary indicate ovarian development prior to thestart of migration (Toste 2001). The environmen-tal cues that might stimulate gonad maturationare not yet described. Preliminary data indicatesthat shorter day lengths (following the summersolstice) stimulate ovarian development (Toste2001). In China, summer rain results in increasedwater flow and lower water temperatures, andthese factors may play a role in triggering gonaddevelopment. However, in California, these mete-orological phenomena occur in fall and winter,by which time the crabs have achieved sexualmaturity.

Initiation of reproductive development mayalso be size-dependent. In preliminary tests, mit-ten crabs below 30 mm CW did not show areproductive response, in terms of gonad matura-tion, to either decreasing day length or tempera-ture (Bauer and Tsukimura 2002). It is possiblethat a minimum size requirement is a precondi-tion for the reproductive cues mentioned above.If minimum size, day length, and temperaturechanges work in combination, a crab would needto be at minimum 30 mm CW shortly after thesummer solstice in order to progress to reproduc-tive maturity.

Downstream migration of the adult crabsLarge Chinese mitten crabs (40–70 mmCW) have been observed to congregate inthe lower freshwater portions of San FranciscoEstuary tributaries in the mid-to late-summer,which we describe as staging behavior (Rudnick2003). This staging behavior may be a sign of thebeginning of downstream migration. Down-stream-migrating adults are collected at watermanagement facilities in the southern end of theSacramento–San Joaquin Delta in Septemberand collections are sustained through October,with stragglers caught through January (Fossand Veldhuizen 2001; Rudnick et al. 2003). Thecrab has been suggested to migrate downstreamvery quickly; in Europe, downstream migrationrates were estimated at 7–12 km/day, and as highas 18 km/day (Panning 1939a; Herborg et al.2003).

It is unclear whether the cue for migration istied to local changes such as precipitation orwater temperature, or a more universal cue suchas day length, or a combination of these factors.Increases in collection rates of downstream

migrating adult mitten crabs in the San FranciscoEstuary have been correlated with a decline inwater temperature at the site of collection (Sieg-fried 1999). In a study of the Japanese mittencrab, Eriocheir japonicus, declining water temper-atures correlated with the patterns of down-stream migration of adult crabs (Kobayashi andMatsuura 1995). In South San Francisco Bay,large numbers of crabs were observed to migratein association with rain events (Culver and Wal-ter 2003). Mitten crabs migrate downstream asadults in the fall across all regions they occur,regardless of the fact that these regions exhibit arange of hydrologic patterns and climates in thefall (Table 3). Given the uniformity in timingamong all populations of mitten crabs (nativeand introduced), a more universal environmentalcue, such as photoperiod, may be the strongestinfluence on the timing of the downstream breed-ing migration.

Adult crabs in their breeding groundsThe location of mating for E. sinensis in Europeand China is suggested to be in saline water(Hoestlandt 1948; Zhao and Du 1988). Of 55female crabs collected from fresh water duringtheir downstream migration to San FranciscoBay, none contained sperm in the sperm recepta-cles, suggesting that mating has not yet occurred(Bauer and Tsukimura 2002). Although it hasbeen suggested that attachment of eggs to pleo-pods requires a saline environment, above 25&(Panning 1939a; Ingle 1986), ovigerous females inthe San Francisco Estuary have been collectedprimarily from San Pablo Bay and South SanFrancisco Bay, and to a lesser extent from SuisunBay and Marsh, in salinities ranging between 0.1and 30&, with a mean salinity at point of collec-tion of 18& (Rudnick et al. 2003).

A wide range of sizes of reproductively matureadults has been reported throughout the world.Adult sizes reported from European populationsrange from 38 mm to more than 84 mm (Pan-ning 1939a; Hoestlandt 1948; Ingle 1986)and sizes in Chinese populations of the crabhave been reported from 38 to over 90 mm(Kobayashi and Matsuura 1995; Jin et al. 1999;Zhang et al. 2001). In a study of cultured Chi-nese mitten crabs in China, only a small subsetwere found to become reproductive at smallersizes, in the range of 30–42 mm (Jin et al. 2001;

345

Zhang et al. 2001). In the San Francisco Estuary,reproductively mature mitten crabs collectedfrom San Francisco Bay range between 30 and95 mm carapace width, but the majority ofadults collected have ranged in size from 45 to70mm (Rudnick et al. 2003).

The average size of reproductively mature mit-ten crabs in the North and South Bay popula-tions has diverged over the period of the crab’sestablishment, so that average sizes of adult crabscollected from the South Bay (mean � 45 mmCW) are significantly smaller than the averagesize of adult crabs collected from the North Bay(mean � 60 mm CW) (Rudnick et al. 2003).Although the reason for this size divergence isunclear, it is consistent with our discussion ofgrowth rates and their variability with differingenvironmental conditions. Some of the tributariesto North San Francisco Bay are deeper than,and are cooler in fall and winter than, manySouth San Francisco Bay tributaries (Orsi 1999;Culver and Walter 2002; USGS 2003). It is possi-ble that these habitat differences translate into aslower growth rate for North Bay crabs, so thatthey do not achieve the minimum size needed tocommence maturation, and they therefore over-winter an additional year, leading to a larger sizeat maturity. Alternatively, the larger molt incre-ment reported for North San Francisco Baycrabs relative to that of South San Francisco Baycrabs (see Age 1 section, above, and Time toMaturity Model, below), could influence the dif-ference in size at sexual maturity. An increasedunderstanding of the association between watertemperature and growth rates of mitten crabsmay help resolve this question.

As discussed in the larval section, femaleE. sinensis may brood the egg cluster for 1–2 months, or egg development could be delayeduntil amenable environmental conditions exist.Given the timing of arrival of recently settledjuveniles and the large range of sizes of age 0crabs found throughout the year in the freshwa-ter tributaries of the San Francisco Estuary, it islikely that the hatching period is extended overseveral months. It has been suggested that adultmitten crabs have a single reproductive seasonand are short-lived after mating (Panning 1939a;Ingle 1986). In support of this hypothesis, wehave never collected live adult male Chinese mit-ten crabs from San Francisco Bay later than

May, with only a small number of adult femalescollected into the early summer (Rudnick et al.2003).

Time to maturity model

Rates of larval and megalopal development

We chose to use Anger’s (1991) rates of larvaldevelopment for the model, as this data set ismore comprehensive over multiple temperaturesand salinities than our laboratory data. However,we documented longer development times foundfor Chinese mitten crab larvae raised from SanFrancisco Estuary crabs, suggesting that Anger’s(1991) data could be conservative for time tometamorphosis (Table 2). During the time thatthe mitten crab has been present in the San Fran-cisco Estuary, temperatures generally have ran-ged between 10 and 20 �C over the course of theyear throughout the open waters of the Bay, andonly reach temperatures as high as 23 �C duringa few weeks in summer in limited areas of theBay (USGS 2003); therefore, Anger’s tested tem-peratures are relevant to the conditions likelyencountered by mitten crab larvae in San Fran-cisco Estuary.

Megalopae raised from the San FranciscoEstuary population of E. sinensis remained in thisstage at a minimum of 21 days at 17 �C and20& in the laboratory, while Anger’s data pro-vides mean megalopal durations of 33 days at12 �C and 25 ppt, to 18 days at 18 �C and25 ppt. If these estimates of megalopal develop-ment time are added to zoeal development time,time to metamorphosis to the juvenile stage (timeto completion of the larval and post-larvalstages) ranges from about 45 to 93 days depend-ing on temperature and salinity (Table 2).

Juvenile growth ratesGiven the timing suggested for larval develop-ment and metamorphosis above, and using theestimated molting rate ((days to stagen+1) ¼ 8.583e0.278 (days to stage n); Figure 3)and molt increments (22%; Figure 4) from labo-ratory studies described above, we constructedmodels of rates of growth over time for juvenileshatched in the early (December 1), mid-(March1), and late (July 1) breeding season to the end

346

of their first year of growth (Figure 7). We usedrates of larval development associated with tem-peratures of 12 and 15 �C for larvae hatching inearly- and mid-breeding season, and rates associ-ated with 15 and 18 �C for larvae hatching in thelate-breeding season, as these temperatures aresimilar to temperature increases in San FranciscoEstuary over the course of the breeding season.Models suggest that crabs hatched early in theseason could reach sizes close to 30 mm CW bythe end of their first year of growth, while crabshatched late in the season may achieve less thanhalf this size in their first year (Figure 7).

This model can inform year class assignmentsfor young juvenile crabs collected from CoyoteCreek (Figure 2): based on model estimates,<5 mm carapace width crabs collected in Aprilfrom Coyote Creek are age 0 crabs hatched inlate winter or early spring. Crabs >10 mm CWcollected early in the sampling period are likelycrabs hatched the previous year. Crabs between5–10 mm CW could be age 0 crabs hatched earlyin the reproductive season or age 1 hatched latein the reproductive season of the previous year.Although our model predicts crabs will be largerthan 10 mm at age 1, if slower fall and wintergrowth rates are factored into the model, it is

possible that some crabs may be smaller than10 mm at age 1.

To estimate growth rates of age 1 crabs, theaverage growth increments of 18 and 26% fromSouth Bay and Delta field data (Age 1 crabs sec-tion) were added to the model. These estimatedvalues were combined with growth rates at vari-ous temperatures of crabs born throughout thereproductive season of the previous year. Crabshatched early the previous year (December hatch)can, in this model, achieve sizes between 33 and50 mm CW by the end of the age 1 calendaryear, while age 1 crabs hatched late in the previ-ous year’s reproductive season (July hatch)achieve sizes between 28 and 38 mm CW by theend of age 1 (Figure 7).

This growth rate model suggests that SanFrancisco Estuary crabs could reach sizesbetween 39 and 78 mm CW by the end of age 2(Figure 7). These sizes overlap with the range ofsizes of adult mitten crabs in San Francisco Bay(see Adults section above). The divergence insizes modeled by incorporating two incrementalgrowth rates also matches the pattern of sizedivergence we have seen in northern and south-ern San Francisco Estuary populations of thecrabs. For all crabs, however, if longer intermoltperiods or smaller growth increments associatedwith lower temperatures are incorporated intothe calculation of rate of growth, crabs at theend of age 2 will be smaller than the estimates inthis model. If a decrease in growth rate duringthe cold season is incorporated into the model,some crabs might not reach reproductive size atAge 2, and may need to overwinter past age 2 toattain a minimum reproductive size.

While this model incorporates variability ingrowth increment (18 and 26%), and the expo-nential equation for juvenile growth rates incor-porates a slowing in molting rate over time, themodel does not account for seasonal variabilityin the intermolt period. Given that growth mayslow, if not cease, during the cooler winter andearly spring months, this model may overestimategrowth rates. The model also does not accountfor the fact that warm temperatures during sum-mer months could, conversely, lead to a shorten-ing of the intermolt period. The sizes we presentin our model, therefore, should be seen as broadestimates likely to be strongly influenced by sea-sonal temperature changes.

DateDec Jun Dec Jun Dec Jun Dec

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Age 1 Age 2

Age 0

Figure 7. Models of Chinese mitten crab growth rates based

on December 1, March 1, and July 1 hatch dates, two temper-

atures during the period of larval development, and two rates

of incremental growth (G.R.). Lower temperatures of larval

development (12 and 15 �C, see Table 2) are used for Decem-

ber and March hatch dates, as these temperatures are charac-

teristic of the range of temperatures in San Francisco Bay

likely encountered by mitten crab larvae in winter and early

spring; while higher temperatures (15 and 18 �C) are used for

temperatures during development of larvae hatched in early

summer.

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Conclusions

Our model supports a life span for the San Fran-cisco Estuary population of the Chinese mittencrab, from hatching to reproductive maturity, of3 years for most crabs (Figure 8). This estimatedlife span for this population of the Chinese mit-ten crab is intermediate to the 4–5 year life cyclereported for colder climates, such as NorthernEurope (Panning 1939a; Gollasch 1999) and the2 year life cycle reported for Chinese populationsof the crab reared in warmer waters (Zhang et al.2001) (Table 3). This gradient of life spans ofboth native and introduced populations of E. sin-ensis supports the hypothesis that the timing ofthe life cycle is strongly tied to environmentalconditions. The tendency of this species toundergo rapid, population-wide fluctuations inabundance also suggests that environmentalparameters play a strong role in governing thecrab’s population dynamics. Further study ofenvironmental parameters on mitten crab popu-lations are warranted, including the effects of:water temperature and salinity on embryonic, lar-val and post-larval development and survival;freshwater discharge on settling patterns and suc-cess of megalopae; water temperature on growthrates of juvenile crabs; day length on maturation;and temperature decreases on downstream migra-tion (Figure 8). The link between minimum sizeand the onset of reproductive maturity shouldalso be further explored, as this relationship

would have a major influence on the length oftime spent in fresh water by the mitten crab and,in turn, the length of the overall life cycle.

In addition to climatic and hydrologic condi-tions of the area, the success of the Chinese mit-ten crab’s establishment and spread in the SanFrancisco Estuary is likely also a function of thisregion’s geography. The enormous estuarine areaof this system provides an abundance of poten-tial spawning and rearing habitat for the crab,and its semi-enclosed shape may play a role inretention of mitten crab larvae. A better under-standing of whether this species has mechanismsfor larval retention would elucidate whether thespecies might do equally well in less protectedestuaries and improve risk assessment for its suc-cess in other regions. Continued examination ofthe factors affecting the population dynamics ofE. sinensis will undoubtedly provide useful infor-mation for managing this invasive species. Forexample, understanding the relationship of watertemperatures and cohort strength could allowbetter predictions of year-class strength andanticipated impacts. Such predictive capabilitieswould directly benefit activities and institutionsimpacted by the crabs, including water facilitiesmanagers in California who must wait for thecrabs to appear before determining whether addi-tional measures must be taken to reduce impactson water pumping and fish survivorship in hold-ing tanks. Commercial and recreational fishermenalso have to currently ‘wait-and-see’ if crab

Figure 8. Conceptual model for the life cycle of the Chinese mitten crab, and major environmental factors that influence the timing

and probability of survival of each stage. P(x) ¼ probability of survival through stage x, as mortality is associated with each stage;

M(x) ¼ fecundity at age x. A dashed line for Age 1 indicates that the contribution of Age 1 crabs to reproduction is unknown but,

if it occurs, is probably quite low relative to older crabs.

348

abundances will impact their activities. Identify-ing cues related to upstream and downstreammigrations would also be useful to these groups,by providing better predictors of when the crabsmay become a problem. More broadly, such pre-dictive abilities would help determine years whendirected management efforts may be criticallyneeded to control populations of E. sinensis.

Acknowledgements

The authors would like to thank Zach Hyman-son, CALFED, for encouraging the developmentof this life history model and providing feedbackon its development; Daniel Bauer, CaliforniaState University, Fresno; Erin Williams, DavidBergendorf, and Kim Webb, US Fish and Wild-life Service; Vincent Resh, University of Califor-nia, Berkeley, for reviewing and discussing thismanuscript; and Richard Moss, CSU Fresno, forassistance gathering literature and proofreading.Thanks to David Salbery, Jae Abel, Lisa Porcella,and Melissa Moore of the Santa Clara ValleyWater District for their support of migration andrecruitment studies. Funding for the research thatsupported the development of this model wasprovided by CALFED, the US Fish and WildlifeService, the California Interagency EcologicalProgram for the San Francisco Estuary, the Cali-fornia Water Institute, and National Sea Grant.

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