Thermal Effects on Embryonic Development and Hatching for Blue King Crab

Paralithodes platypus (Brandt, 1850) Held in the Laboratory, and a Method for
Predicting Dates of Hatching
Author(s): Bradley G. Stevens, Katherine M. Swiney, Loren Buck
Source: Journal of Shellfish Research, 27(5):1255-1263. 2008.
Published By: National Shellfisheries Association
DOI: http://dx.doi.org/10.2983/0730-8000-27.5.1255
URL: http://www.bioone.org/doi/full/10.2983/0730-8000-27.5.1255

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Journal of Shellfish Research, Vol. 27, No. 5, 1255–1263, 2008.

THERMAL EFFECTS ON EMBRYONIC DEVELOPMENT AND HATCHING FOR BLUE KING

CRAB PARALITHODES PLATYPUS (BRANDT, 1850) HELD IN THE LABORATORY,
AND A METHOD FOR PREDICTING DATES OF HATCHING

BRADLEY G. STEVENS,1 KATHERINE M. SWINEY2 AND LOREN BUCK3

1
School of Marine Science and Technology, University of Massachusetts Dartmouth, 706 S. Rodney
French Blvd, New Bedford, MA 02744; 2National Marine Fisheries Service, Alaska Fisheries Science
Center, Kodiak Fishery Research Center, 301 Research Ct., Kodiak, Alaska, 99615; 3University of
Alaska, Anchorage, Anchorage Alaska 99501

ABSTRACT Climate change may affect crab populations via thermal effects on embryo development and hatching. To test this,
we measured the duration of development and hatching for the embryos of 11 blue king crabs Paralithodes platypus held at 2.3 ±
0.45, 4.3 ± 0.31, and 6.1 ± 0.61°C. Embryo area, length, and width, eye length and width, and percent yolk were measured biweekly
from digital images, and hatching larvae were collected daily from individual crabs. Data were compared between eggs of identical
age (weeks since fertilization). Temperature did not have a significant effect on embryo measurements, but did affect development
indices (percent yolk and eye size). Hatching was significantly delayed at colder temperatures with about a 46-day difference from
2.3°C to 6.1°C. Length of development was related to temperature via a power function, and ranged from 410 ± 8 days at 6.1°C to
434 ± 11 days at 2.3°C. Length of hatching increased from 40 ± 4.6 days at 2.3°C to 55 ± 6.2 days at 6.1°C. A model for predicting
hatching dates from an eye index was developed using a quadratic equation. Embryo development at 4.3 and 6.1°C was arrested
between weeks 35 and 50; this evidence, plus other behavioral observations, suggests that crabs may be able to adjust development
rates to partially compensate for temperature changes.

KEY WORDS: blue king crab, Paralithodes platypus, decapoda, anomura, hatching, embryo development, temperature

INTRODUCTION 1990). Hatching of RKC is delayed in years with particularly

low water temperatures (Otto et al. 1990, Shirley et al. 1990). A
Blue king crabs (BKC) Paralithodes platypus (Brandt, 1850)
mismatch between the timing of hatching and the presence of
are commercially valuable crustaceans in the Pacific Ocean
food sources (e.g., the phytoplankton bloom) could lead to
waters of Alaska, Japan and Russia. Declines in abundance in
subsequent starvation and year-class failure (Hjort 1914, Cush-
Alaska have led to closures of commercial fisheries in the
ing 1990). Recent studies have demonstrated marked warming
Pribilof Islands and at St. Matthew Island since 1999 (NPFMC
trends in the Bering Sea (Overland & Stabeno 2004). In cold
2002). Populations of other crab species in Alaska, including the
years with normal sea ice cover during March to April, a sharply
red king crab (RKC) Paralithodes camtschaticus (Tilesius,
defined early spring phytoplankton bloom occurs, whereas in
1815), have also fluctuated greatly over the last three decades.
years with warmer temperatures (and the absence of ice) the
Among several explanatory hypotheses put forward, the most
phytoplankton bloom is delayed until May/June (Stabeno et al.
plausible include highly variable recruitment of juveniles asso-
2001). Therefore, earlier hatching of crab larvae as a result of
ciated with climatic change (Zheng & Kruse 2000), and indirect
warmer temperatures may be more likely to cause a mismatch
effects of spatial distribution of adults on larval survival (Loher
with food sources.
& Armstrong 2005).
To investigate the effects of climate change on crab recruit-
Female BKC become sexually mature at a size of 96.3 mm
ment processes, we held blue king crabs at three different
carapace length (CL) in the Pribilof Islands, but only 80.6 mm
temperatures to determine how embryonic development rates
at St. Matthew Island (Somerton & MacIntosh 1983). Female
and hatch timing were affected by temperature. In particular,
BKC in the Bering Sea have a biennial reproductive cycle
we wanted to know if increased temperatures would result
(Somerton & MacIntosh 1985, Jensen & Armstrong 1989).
in faster development and earlier hatching with a shorter
Adult females molt, mate, and extrude fertilized embryos in the
duration.
late winter or early spring (February to March). Embryonic
development requires 13 mo and has 12 identifiable stages
(Stevens 2006a). Larval hatching occurs in the late spring MATERIALS AND METHODS
(March to April) and requires about 30 days per female (Stevens
2006b). Females carry empty egg cases for another year until Crab Treatments
they spawn again the following spring (Somerton & MacIntosh
1985). Ovigerous female BKC were captured near the Pribilof
Hatching is a critical early event in the life of king crabs, and Islands (between 56°54’ and 57°35’ N, and between 169°18’
timing of hatching may have significant impact on their and 169°30’ W) in September 2003 using side-loading crab pots,
survival. Stage 1 zoea of RKC must find adequate food sources and returned to Dutch Harbor, AK, aboard ship. Crabs were
such as diatoms (Thallasiosira sp.) and feed within 3 days of then packed in wet burlap bags with gel ice and shipped to
hatching or survival will be poor (Paul et al. 1989, Paul & Paul Kodiak in large coolers; on arrival in Kodiak they were placed
in a 4,000-L tank with recirculating chilled seawater at 4°C. All
*Corresponding author. bstevens@umassd.edu crabs were measured from the right orbit to the rear center

1255
1256 STEVENS ET AL.

margin of the carapace (carapace length, CL) using vernier

calipers. All female crabs hatched larvae in the spring of 2004
(Stevens 2006b) and did not molt or spawn again until the
following winter. In January 2005, prior to molting, 12 females
were randomly divided into three groups of four crabs each, and
placed into tanks of seawater chilled to set-points of 2, 4, or 6°C
(hereafter referred to as the 2C, 4C, and 6C treatments). These
temperatures were selected because they encompass the range of
depth-averaged temperature on the Bering Sea shelf from 1998–
2004 (Overland & Stabeno 2004). Crabs in the 2C and 6C
treatments were held in separate 2,500-L tanks, and the 4C
crabs were in a 4,400-L tank. Each tank had a small amount
(<1 L/min) of ambient water influx to replace stale water. Water
temperatures in each tank were recorded by Onset Water-Temp
Pro electronic temperature loggers (Onset Corporation, P.O.
Box 3450, Pocasset, MA 02559) (Reference to trade names does
not imply endorsement by the National Marine Fisheries
Service, NOAA). Male crabs were also placed into the tanks, Figure 1. Mean daily temperatures (°C) in each of the experimental tanks
and mated with females after they molted. Dates of mating and for blue king crabs. Overall mean temperatures were 2.3, 4.3, and 6.1°C, in
oviposition were recorded. All females except one (in the 2C the 2C, 4C, and 6C tanks, respectively.
treatment) molted, mated, and produced fertilized clutches in
the spring of 2005. Crabs were fed twice weekly ad libitum with a
were compared with eggs that hatched on April 1 and were
combination of squid Loligo spp., herring Clupea harengus,
sampled on May1. Our intent was to determine if there were
Pacific cod Gadus macrocephalus, or coho salmon Oncorhynchus
developmental differences between eggs of the same age at
kisutch cut into 2 cm chunks.
different temperatures.
Eggs were removed from each crab for sampling a total of
Embryo Development 34–36 times (depending on length of development). For this
reason, data were analyzed using a repeated measures general
Development of fertilized eggs was monitored weekly for the
linear model (RM-GLM), with temperature as a fixed factor,
first 6 wk after oviposition, then biweekly until hatching, using
crabs nested within temperatures, and eggs as replicates. Each
methods described previously (Stevens 2006a). A small cluster
measurement (A, L, W, MD, eL, eW, and PAY) was analyzed
of 50–100 eggs was removed from the outer margin of the egg
separately. For A, L, W, and MD, all samples were used, but eL
mass, placed on a glass slide in 1 mL of filtered seawater under a
and eW were only compared after week 12, and PAY only after
compound microscope at 3 50 magnification, and 10 eggs were
week 22, to exclude most weeks when values were identical (0 or
digitally photographed with a 2 megapixel digital camera
(Diagnostic Instruments Spot Insight camera) using reflected
light (darkfield background). Eggs were only photographed if
they were rotated at 90° to the sagittal plane. Eggs were
measured using Image-Pro Plus, version 4.5, after calibration
with a stage micrometer. Measurements were made by outlining
the embryo on the computer screen using a digital drawing pad
and pen, with automatic tracing and a smoothing value of 5.
For the first 3 mo, digital measurements were made of egg area
(A), maximum diameter (L), minimum diameter (W) and mean
diameter (MD, calculated from 180 measurements taken at 2°
intervals around the perimeter). After embryos became appar-
ent, the areas of the embryo and yolk mass were determined,
and the percentage of apparent cross-sectional area occupied by
yolk (PAY) was calculated. After eyespots became apparent, 10
additional embryos were photographed with the eyespot cen-
trally positioned, and L and W of the pigmented eyespots (eL
and eW, respectively) were measured. Measurements were
output directly to an Excel spreadsheet for analysis. An eye
development index (eI, Perkins 1972) was also calculated for
each sample as (eW + eL)/2.
Prior to statistical analysis, sampling dates were converted to
‘‘egg-age’’ in days by subtracting the date of oviposition from
the date of sampling. Because crabs oviposited on different
dates, comparisons were made only between eggs of the same Figure 2. Mean egg area (mm2) at two-week intervals of egg age for blue
egg-age, rounded to the nearest week. Thus, eggs that hatched king crab embryos at each experimental temperature. Vertical bars are
on February 1 and were sampled on March 1 (egg-age 4 wk) %1 SD.
 BLUE KING CRAB HATCHING 1257

TABLE 1A.
Repeated measures GLM of blue king crab embryo measurements. B(A) indicates the effect of Factor B (crabs)
nested within Factor A (temperature).

Egg area Max diameter Min diameter Mean diameter

(A) (L) (W) (MD)
Source DF F P F P F P F P
A: DegC 2 0.9 0.4457 0.8 0.4979 1.6 0.2625 0.9 0.4537
B(A): Crab 8 169.4 <0.0001 103.7 <0.0001 54.0 <0.0001 165.3 <0.0001
C: Week 33 313.7 <0.0001 178.7 <0.0001 210.2 <0.0001 315.3 <0.0001
AC 66 4.2 <0.0001 3.1 <0.0001 2.4 <0.0001 3.9 <0.0001
BC(A) 243 4.2 <0.0001 2.9 <0.0001 2.2 <0.0001 4.0 <0.0001
S 3,182
Total (Adjusted) 3,534

1, respectively). Posthoc comparisons between temperature
groups were conducted with Tukey HSD test and differences
were considered significant if P < 0.05. Mean values ±1.0 SD are
given where appropriate. Analyses were conducted with SAS
version 9.
Hatching Studies
Several weeks prior to hatching (as estimated by egg
measurements), female crabs were placed into individual 70-L
plastic tubs within the chilled tanks, and each tub received
flowing chilled seawater at a rate of 4–5 Lmin–1. Larvae
hatched during the first few hours of darkness each evening
(similar to red king crab, Stevens & Swiney 2007), and were
washed out through a drain on the lower sidewall of the tank
and into a fine mesh net. The net was removed daily and larval
volume measured to the nearest 0.5 mL in a graduated cylinder.
When <0.5 mL was present, larvae were counted individually. A
linear relationship between volume and number of hatched
BKC larvae has previously been established (Stevens 2006b).
Mean hatching date for each crab was determined as the
weighted average of larval production over time, that is, by
multiplying the daily volume of hatched larvae by day-of-the-
year (DoY), summing the products over time and dividing by
total volume of larvae released; however, this method does not
allow determination of a standard deviation for each crab.
Total hatching days were defined as the number of continuous
days on which each crab released more than 0.1 mL (approx-
imately 30 larvae). Development days were defined as the
difference between the date of oviposition and mean hatching
date. Degree-days accumulated by each crab were the sum of
mean daily water temperatures over the development period for
each crab, assuming 0.0°C as the threshold temperature, or
‘‘biological zero.’’
Mean dates of oviposition and hatching (as DoY), total
hatching days, total development days and degree days, and
total volume of hatched larvae were compared with holding
temperature by linear regression analysis; there were not
enough data to determine whether nonlinear analysis would
provide a better fit. However, the relationship between temper-
ature and egg development time was fit to the power function of
Belehradek (Hartnoll 1982).
V ¼ a  ðT + aÞb

TABLE 1B.
Repeated measures GLM of blue king crab eye measurements
after week 22.

Eye length Eye width

(eL) (eW)
Source DF F P F P
A: DegC 2 93.3 <0.0001 77.8 <0.0001
B(A): Crab 8 91.6 <0.0001 107.2 <0.0001
C: Week 19 661.7 <0.0001 1,504.2 <0.0001
AC 38 49.2 <0.0001 117.0 <0.0001
BC(A) 145 9.5 <0.0001 4.1 <0.0001
Figure 3. Mean eye length (mm) at two-week intervals of egg age for blue S 1,903
king crab embryos at each experimental temperature. Vertical bars are Total (Adjusted) 2,115
%1 SD.
1258 STEVENS ET AL.

where V is velocity (D–1), T is temperature and a, b, and a are

constants. When inverted and linearized, this equation
becomes:
logðDÞ ¼ logðaÞ + b  logðT+aÞ
However, the scaling factor a, which represents a ‘‘biological
zero’’ at which no development occurs, is usually incorporated
within T. Nonlinear regression was used to fit the eye develop-
ment index (eI) to the number of days remaining (Dr) until
hatching, because it eliminates transformation errors produced
by linearization. Data at each experimental temperature were fit
to a separate quadratic equation and a combined equation with
additional terms for temperature was also calculated. Nonlinear
regression models were fit using Systat 11 (SYSTAT 2004).
Where appropriate, values are given as mean ±1 SD.

RESULTS

Mean water temperatures during the course of the experi-

ment in the 2C, 4C, and 6C treatment tanks were 2.3 ± 0.45, 4.3
± 0.31, and 6.1 ± 0.61°C, respectively (Fig. 1), and daily means
were significantly different (ANOVA, F ¼ 7,795, P < 0.0001).
Summer temperatures were least stable because of the influx of Figure 4. Mean percent area of yolk (PAY) (mm2) at two-week intervals
of egg age for blue king crab embryos at each experimental temperature.
warmer makeup water.
Vertical bars are %1 SD.
Mean egg area (over all temperatures) was initially 0.92
mm2, declined to about 0.82 mm2 at week 10, then increased to
about 1.3 mm2 at week 60 (Fig. 2). Temperature did not have a
significant effect on egg area, L, W, or MD of the eggs, which all 130.6 ± 3.7, and was not significantly different between groups
followed similar trends (Table 1A). However, there were (F(2,8) ¼ 0.61, P ¼ 0.565, Table 2). Mean day-of-the-year for
significant differences between crabs within temperatures, and oviposition (Ovip DoY) was about 1 wk earlier for each degree
between weeks, as expected. There were also significant inter- of temperature increase (Fig. 5), but the difference was not
actions between weeks and temperature, and between crabs and significant (Table 2). Crabs had been placed in the experimental
weeks within temperatures. These differences primarily arose temperatures in January 2005, so temperature effects did not
from differences in timing of molting, mating, and oviposition encompass the entire period of ovarian development prior to
between the different crabs and temperatures. oviposition. However, after being held at experimental temper-
The crescent-shaped eye first appeared at a starting length of atures during the entire embryo development period, mean
about 0.15 mm at egg-ages of 26, 30, and 38 wk in the 6C, 4C, dates of hatching (Hatch DoY) were significantly related to
and 2C treatments, respectively (Fig. 3). Growth of the eyes temperature (Table 3); hatching was delayed at colder temper-
increased significantly with temperature, which had a significant atures (Table 2), with a mean difference of 46 days from 2°C to
effect on both eL and eW (Table 1B). All three temperature 6°C. Mean dates of hatching were February 28, March 18, and
groups were significantly different from each other. Again, there April 15, 2006, for the 6C, 4C, and 2C groups, respectively.
were significant effects for crabs, weeks, and the interactions of Mean development days were significantly inversely correlated
weeks with crabs and temperatures. with temperature (Fig. 6, Table 3), and ranged from a mean of
Percent area of yolk (PAY) declined as embryos developed,
so can be used as a proxy for developmental stage (Fig. 4). PAY
also differed significantly with temperature (Table 1C), and the
effects of crabs, weeks, and their interactions were all signifi- TABLE 1C.
cant. Embryos developed earlier at higher temperatures, and Repeated measures GLM of blue king crab yolk area
between weeks 20 and 36 development was most rapid in the 6C measurements after week 12.
group, and less so in the 4C and 2C groups. After reaching an
egg-age of 34 wk, the development rate of embryos in the 6C Percent area
and 4C groups slowed down, but that of the 2C group did not yolk (PAY)
(Fig. 4). By the time that embryos reached the egg-age of 50 wk,
Source DF F P
and from then until hatching, there was little difference between
the groups. Mean PAY for 2C crabs was significantly different A: DegC 2 23.8 <0.0001
from that for 4C and 6C crabs, but the latter two groups were B(A): Crab 8 163.2 <0.0001
similar. Between-week effects were significant for all measure- C: Week 24 1,265.8 <0.0001
ments, as expected. However, there were also significant AC 48 13.7 <0.0001
BC(A) 185 6.9 <0.0001
between-crab effects as well (Table 1C).
S 2,412
Variances for all hatching parameters were homogeneous Total (Adjusted) 2,679
(Levene test, P > 0.05). Mean carapace length of crabs was
 BLUE KING CRAB HATCHING 1259

TABLE 2.
Mean values (%1 SD) of hatching parameters for blue king crab embryos at different temperatures. CL, Carapace length;
Ovip DOY, oviposition day-of-year; Hatch DOY, mean date of hatching; Dev-days, total development days; Hatch Days,
number of days on which hatching occurred; Volume, total volume of hatched larvae (mL).

Degrees C CL (mm) Ovip DOY Hatch DOY Dev-Days Degree Days Hatch Days Volume (mL)
Mean (±SD) 2.34 (0.45) 128.5 (0.92) 36.7 (22.50) 105.5 (16.8) 433.8 (11.0) 1,014.9 (25.6) 40.0 (4.6) 369.6 (150.5)
Mean (±SD) 4.26 (0.30) 131.1 (5.58) 27.0 (17.19) 77.3 (13.9) 415.3 (9.3) 1,769.3 (40.0) 43.3 (7.0) 348.5 (146.6)
Mean (±SD) 6.11 (0.61) 131.7 (2.82) 14.8 (12.84) 59.8 (17.6) 410.1 (7.7) 2,503.1 (49.6) 55.3 (6.2) 342.7 (141.0)
Overall Mean 130.6 (3.70) 25.18 (17.99) 78.6 (23.8) 418.5 (13.1) 1,830.4 (619.2) 46.7 (8.8) 352.1 (130.7)
ANOVA F 7,795 0.61 1.41 6.77 6.07 1,211.6 6.22 0.03
ANOVA P <0.0001 0.565 0.299 0.019 0.025 0 0.024 0.969
Levene’s X2 3.447 0.285 0.339 0.038 0.156 0.453 0.002
Levene’s P 0.083 0.759 0.722 0.963 0.858 0.651 0.998

410 at 6°C to 434 at 2°C. However, this range (24 d) was half of
that for hatching dates. Mean total degree-days accumulated
during development were 1,015, 1,770, and 2,503 for the 2C, 4C,
and 6C groups, respectively, (with little variance, Table 2) and
were significantly correlated with temperature (Fig. 6, Table 3);
they are essentially equal to mean development days multiplied
by holding temperature. Number of hatching days was also
significantly correlated with temperature (Table 3), and ranged
from a mean of 40 days at 2°C to a mean of 55 days at 6°C (Fig.
7). Total volume (hence, number) of larvae released did not
differ significantly between groups (Fig. 8); one crab in each
group had a clutch that was significantly smaller than the other
crabs.
Mean development times for each crab were significantly
correlated with temperature when their relationship was
expressed as a power function (where Days are total develop-
ment days, and T is degrees Celsius) (Fig. 9):
Days ¼ 455:23  ðT0:0592 Þ ðn ¼ 11; R2 ¼ 0:584; P < 0:01Þ
It was also possible to predict the number of days remaining to
hatching (Dr) from the eye index (eI) using a quadratic equation
(Fig. 10). At the specific experimental temperatures used, only
parameters b1 and c1 are required (Table 4). A comprehensive
equation incorporating a Temperature component (T) required
the inclusion of associated parameters b2 and c2:
Dr ¼ a + b1 eI + c1 eI2 ð+ b2 T + c2 T2 Þ:
DISCUSSION
Temperature has significant effects on the processes of
embryonic development and hatching in blue king crabs. This
conclusion is almost certainly true for other king crabs, and
highly probable for other crabs in general. That is not surpris-
ing; the rates of biochemical (and physiological) processes are
dependent on temperature, and growth rates are related to
temperature via the power function of Belehradek (Hartnoll
1982). Kurata (1960, 1961, 1962) and Nakanishi et al. (1974,
1987) studied the growth of red king crabs and found that
intermolt period for a given instar decreased with temperature
at a constant rate, and concluded that the number of degree-
days (or days  °C) were constant for a given instar (implying
that b, the exponent of the growth function, was equal to 1).
Stevens and Munk (1990) studied growth of juvenile red king
crabs at Kodiak, AK, and developed an equation to predict size
from temperature. All of the above studies concluded that
degree-days would be constant across temperatures and result
in decreasing intermolt periods (i.e., faster growth) with
increasing temperature.
The results of this study conflict with the conclusions of
previous studies of king crab growth. All crabs had been held at
6°C during the previous year, and were only exposed to

TABLE 3.
Regression parameters for blue king crab hatching data versus
temperature. Ovip DOY and Hatch DOY are dates of oviposition
or mean hatching date, respectively, as day-of-year.

Regression data a b R2 F P
Ovip DOY 51.0 –5.85 0.2589 3.144 0.110
Hatch DOY 131.5 –11.99 0.6230 14.873 0.004
Development days 445.5 –6.14 0.5420 10.651 0.010
Degree Days 87.7 394.93 0.9964 2,522.8 0.000
Hatching Days 28.4 4.15 0.5410 10.609 0.010
Figure 5. Dates of hatching and oviposition (as day of year, DoY) for blue Total mL 382.9 –6.96 0.0069 0.063 0.807
king crabs at each experimental temperature.
1260 STEVENS ET AL.
Figure 6. Number of degree-days and development days for blue king
crabs at each experimental temperature.
temperatures of 4C and 2C for 3.5 and 4.5 mo, respectively,
before oviposition. Temperature-dependent embryo develop-
ment resulted in significant delays in hatching at lower temper-
atures. However, if degree-days required to reach a specific
developmental stage (hatching) were constant across temper-
atures (as predicted by previous studies) then the time required
for development, and subsequent differences between dates of
hatching, should have been much greater. For example, if
degree days required for complete embryonic development were
a constant value of 1,800, then development should have
required 900, 450, or 300 days at 2, 4, or 6°C. Instead,
development times differed by only 24 days over the 4°C range
of temperatures. Furthermore, the data provided a significant
nonlinear fit to the Belehradek equation. Our results suggest
that degree days for development are not constant across
temperatures for a given instar, but rather follow a nonlinear
power relationship.
Development rates for embryos and larvae of other large
crustaceans, such as the American lobster Homarus americanus,
Figure 7. Number of hatching days for blue king crabs at each experi-
mental temperature.
Figure 8. Volume of hatched larvae for blue king crabs at each
experimental temperature.
are also highly temperature dependent (Perkins 1972, Char-
mantier & Mounet-Guillaume 1992). Perkins (1972) developed
an eye index (the average of eye length and width) for American
lobster, and used it to predict hatching dates of embryos.
Charmantier and Mounet-Guillaume (1992) indicated that the
lobster eye index develops at a relatively constant rate over time
(although only a predicted line was shown without raw data).
However, the eye index of BKC develops in an asymptotic
fashion, so is not as good a predictor of hatching date as percent
yolk area, which changes rapidly toward the end of develop-
ment. Nonetheless, for comparative purposes, we chose to
model hatch timing using the methods developed for American
lobster by Perkins (1972) and Charmantier and Mounet-
Guillaume (1992). Additionally, eye measurements are easy to
obtain without sophisticated digital image analysis systems, and
it can be used by biologists in the field to estimate developmen-
tal stage and time to hatching. Tong et al. (2000) studied the
effect of temperature on development of embryos of the rock
lobster Jasus edwardsii and concluded that a constant value of
Figure 9. Regression of development days versus degrees C for blue king
crab embryos. Each data point represents a single crab. Regression
equation is: Days $ 455.23  (T0.0592) (n $ 11, R2 $ 0.584, P < 0.01).
 BLUE KING CRAB HATCHING 1261

optimum development time for blue king crab larvae of about

418 ± 13 days (the overall average). Furthermore, it suggests
that differences in growth rates may not be due solely to
biochemical effects of temperature, but that the crabs or their
embryos may take an active role in adjusting development rates
to reduce variance in hatch timing caused by environmental
variation. In addition, rates of development appeared to
become less sensitive to temperature as the embryos neared
hatching.
Embryo development rates may be a property of the species,
subject to some environmental control. Whereas temperature
clearly affects development, access to oxygen may also be a
controlling factor. King crabs have the longest hatching times
of any crabs studied to date, approximating one month for blue
(Stevens 2006b), red (Stevens & Swiney 2007), and southern
king crabs (Lithodes centolla) (Thatje et al. 2003). This extended
hatch timing may be preprogrammed to disperse larvae over a
wide temporal window (the diversified bet-hedging hypothesis,
Stevens 2006b), or may be a function of oxygen gradients within
Figure 10. Days remaining to hatch versus eye index for blue king crab the egg mass as proposed by Thatje et al. (2003). Baeza &
embryos. Crabs were sampled biweekly producing multiple points per Fernandez (2002) demonstrated in the crab Cancer setosus that
crab. See Table 4 for nonlinear regression parameters. oxygen availability in the center of the egg mass increased
during abdominal flapping, and both the frequency of flapping,
‘‘Effective Accumulated Temperature’’ (equivalent to degree- and oxygen demand of crab embryos, increased with embryonic
days) could be used to predict development time at any development. Oxygen availability (as pO2) decreases as it is
temperature. However, rock lobster did not develop below a consumed by embryos, and is replenished by abdominal
biological zero of 7.53°C, and the temperature-development flapping of the adult, resulting in a cyclic pattern in early-stage
relationship was much steeper than for blue king crabs. embryo masses, but in later-stage masses, pO2 was constantly
Application of their approach to BKC predicted a biological high because of increased abdominal flapping frequency
zero of –33°C, which is clearly meaningless. (Fernandez et al. 2002). Furthermore, a gradient in pO2 was
Development rates of crab embryos were not constant observed from the outside to the inside of the egg mass, and this
over time within any experimental temperature, as shown by resulted in delayed hatching of innermost embryos (Fernandez
changes in percent area of yolk (PAY, Fig. 4). Embryos at 2°C et al. 2003). We have also observed oxygen gradients in blue
developed at a fairly constant rate from egg-ages of 30–60 wk, king crab egg masses that vary with maternal pleopod fanning
whereas those at 4°C and 6°C exhibited reduced development (unpublished data). This demonstrates that crabs can actively
from weeks 35–50. This slowing of development has often adjust the delivery of oxygen to attached embryos, which
been termed diapause, and is exhibited by snow crab Chionoe- probably results in adjusting developmental rates as well.
cetes opilio (Moriyasu & Lanteigne 1998) and Tanner crab (C. Why or how crabs determine when to make such adjustments
bairdi) (Swiney 2008). The end result was that mean develop- is unknown, but may be a response to the concentration of CO2
ment times differed by only 24 days among the three temper- or other metabolites produced by embryos. Regardless of the
ature groups. These observations suggest that there is an mechanism, the end result for blue king crabs was reduced
variability in hatch timing between temperature groups,
compared with what might have occurred without such
adjustments.
TABLE 4.
One unexpected result was the positive correlation between
Parameters of nonlinear quadratic regression for predicting days temperature and number of hatching days. Tlusty et al. (in
remaining to hatch (Dr) for blue king crabs from eye index (eI) press) observed a similar response in American lobsters held at
and temperature (T) as degrees Celsius. The regression equation elevated temperatures, and attributed this to the absence of an
for each temperature is Dr $ a + b1eI + c1eI2 . The parameters
abrupt temperature increase that occurs in ambient water
(+ b2T + c2T2) are required only for extrapolating between
those tempearatures. conditions and helps to synchronize hatching. Lobster embryos
cease developing below 5°C (Perkins 1972), and begin rapid
development when temperature rises above 10°C (Helluy &
DegC 2.3 4.3 6.1 All Beltz 1991), eventually hatching in early to midsummer.
Parameter
However, unlike lobsters, there is no evidence that king crab
a 191.01 169.29 138.67 71.585 embryos stop developing at low temperatures (within their
b1 23.485 755.84 1,512.6 840.934 normal environmental range of 0°C to 10°C), and hatching
c1 –1,484.4 –3,607 –5,783 –3,838.79 typically occurs during the coldest part of the year (Stevens
b2 0 0 0 33.067 2006b, Stevens & Swiney 2007).
c2 0 0 0 –2.682
Hatch timing has important implications for survival of crab
N 41 65 71 177
R2 0.9726 0.9416 0.8995 0.888
larvae. Red king crab larvae must find food (diatoms of
Thallassiosira sp.) within 3 days of hatching or survival
1262 STEVENS ET AL.
decreases dramatically (Paul & Paul 1980). Hatching too early
or too late could result in missing the primary peak of diatom
blooms, and subsequently poor survival, according to the
‘‘match-mismatch’’ hypothesis (Hjort 1914, Cushing 1990,
Cushing & Horwood 1994). Diatom blooms in the Bering Sea
have been shown to be highly dependent on water temperature.
In cold years with ice cover, blooms occur early (March to
April), but in warmer years they occur later (May to June)
(Stabeno et al. 1998, Stabeno et al. 2001). Recent warming
trends have resulted in higher temperatures and less ice cover
than ever previously recorded. Summer water temperatures
were 2°C warmer in the period 2001 to 2003 than in the period
1995 to 1997, and since 2000, ice cover has been practically
absent between 57° and 58° N (Overland & Stabeno 2004).
Later phytoplankton blooms support higher levels of zooplank-
ton (Overland & Stabeno 2004) that may compete directly with
king crab larvae for food. King crabs are probably adapted to
the cold environment of the Bering Sea, and typically they hatch
in March to April when diatom blooms are peaking (a
‘‘match’’). If warmer temperatures produced earlier hatching
of crab larvae, along with delayed development of blooms, it
would result in a ‘‘mismatch’’ leading to poor survival and
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