ever,
higher
1960; where Bowler,
Temperature
Introduction
15
rate
Emlet
than at
field
177 A.
1987).
significant ture
of
and
a many characteristics,
rate.
ment, evidence
British
hand,
seasonal from
southeast
“northern”
In
report
suggest
ment adapted
cal
shows
ABSTRACT
A.
Richard
Nucella to
given
Temperature
development that
et
spite
Marine
has
dependence, rate
processes
A
al..
Richard
Maturity:
other
Barkley
as
In
rate
can
Columbian
of
review
here
little
a of of
temperature
well
Palmer.
addition, rather
organisms.
for
Station,
1987;
variation
warm-adapted
profound
constraints
development. this
of
Alaska
Nucella
be
marine
that
evidence
intraspecific
as
development
and
Sound,
of Unlike
explained
close
at
strong
direct-developing
evidence
Johnston,
Department
appears
the
the
Bamfield,
Palmer
suggests
snails
the
hatched
organisms Geographic
emarginata,
many in
a
rate
agreement,
literature
impact
Sensitivity,
As
most
on laying of
same
British
the
Cross-Phyletic
taxon-dependent
a
temperature
(Q
This
the
of
to for
on
latitudinal
consequence,
ones.
British
rate
of
(1/days
that
1990;
other
in development
show
geographic frequency
temperature
the
rate
on
values Zoology.
slower
Columbia.
but
significantly
suggests
encapsulation
of
lies
the
In
however,
basis Columbia
also
of
but physiological
muricacean
little
exhibit
a
to
very
temperature
contrast
development.
of
Variation
rates
physiological rate
compensation—the
Rate
see
hatch) University
exhibit
2.63
of
was
if
that,
variation
constraints
near
a
Over
of
in
McLaren
to
any
taxonomic
VOR
substantial
the
less
at
of
versus
development, the
more
Overview
proceed
was
a
to
temperatures
of
in
that
many
temperature during
phenomenon
gastropods
more
a
lBO.
time
of
laboratory
spite
processes,
most
compensation
rather
Development,
less
in
Alberta,
predicted
pronounced
in
4.66,
the
on
et
precise
process
(up
physiological
the
of
affinity
more
Laboratory-Reared
sensitive
fraction
other
al.,
the
temperature
considerable
narrow
respectively).
to
entire
Edmonton,
tendency,
coupled
of
not
duration
1969).
15 less
rapidly
from
compensation
the
relationship
physiological
and
a
of
in
of
percent
only rocky-shore
in
prejuvenile
to
in
temperature
temperature than
rate
the
cold-adapted
other
Alaskan
temperature.
the temperature
with
So
in
develop
of
Alberta
variation
processes
for
sensitivity
of
10°C,
cold-adapted
variation
average
and
pervasive
These the
muricacean
less
more
example,
development
between
prehatching
snails.
period
T6G
N.
thaidine
(Patel
at
processes,
Time
more
precise
data range
in
compensation,
emarginata
8°C)
rate
of
in
in
These
organisms (Cossins
rate
2E9,
is development
for
Alaskan
reproductive
temperature On
may
thus
and
slowly
gastropods.
of
the
than
than
(8°—i of
gastropod,
physiologi
and
tempera
the
develop
generally
develop
impose
Crisp,
period. patterns
provide
effect
how
Barn-
snails warm-
other
than
and 1°C),
than
from
is I 178 Larval Morphology and Evolution Temperature Sensitivity of Development Rate 179 of temperature on development that, to a reasonable approximation, one can predict the develop Table 15.1. Approximate schedulefor monitoringvariousaspectsof reproductionand growth ment time of species of meso- and neogastropods simply by knowing their taxonomic affinities in laboratory-rearednorthernNucella emarginata and their temperature of development (Spight, 1975). Many marine invertebrates lay their eggs as gelatinous masses or enclosed in egg capsules Period of study eggs in masses or in Aspect of rearing procedure attached to the substratum (Strathmann, 1987). Unlike solitary pelagic eggs. 1982—84 1985—86 1987—92 respiratory gases. and ions because capsules experience limited rates of diffusion of metabolites. Check for egg capsules produced by parents I week 2 weeks 3 weeks of the medium by which they are surrounded and because of their proximity to other developing Duration of capsules in mesh bags 80 days 70 days 70 days embryos (Strathmann and Strathmann, 1989). Encapsulation of embryos is particularly common Check cages for hatching and replenish small 2 weeks 3 weeks 4 weeks among meso- and neogastropods (Strathmann, 1987), yet surprisingly little is known about its barnaclesfor hatchlingsnails fecundity or rate of development (Grahame and Branch, 1985; but see Size at which hatchlings were transferred to cages costs in terms of reduced 3—8mm 3—10mm 3—15nim Perron, 1981b). with larger mesh and larger barnacles Replenish barnacles for juvenile snails Species with limited gene flow should be more likely to exhibit geographic differentiation in 3 weeks 4 weeks 6 weeks Size at which male and female juveniles were response to different climatic regimes than species with greater dispersal potential. Prior studies 15—22mm 15—22mm 15—22mm isolated into separate cages on temperature compensation of development rate have examined species with moderate to high Replenish barnacles for adult snails and check for dispersal potential, including barnacles (Patel and Crisp, 1960), copepods (McLaren et al., 1969), 3 weeks 4 weeks 6 weeks production of capsules echinoderms (Emlet et al., 1987), and fishes (Johnston, 1990). To assess the extent of latitudinal physiological adaptation of development rate in a species with limited dispersal capability, I examined data from the rocky-shore thaidine gastropod “northern” Nucella elnarginata that were Sources of Snails and Rearing Procedure collected as part of a long-term study of the genetic basis of shell variation (Palmer, l984a, Snails were collected from several localities on the Pacific coast of North America, but extensive 1985a,b). Successive generations of snails were reared in the laboratory for over ten years, and sea data were only available for two: (1) Torch Bay, southeast Alaska (58°l9’41” N, l36°47’56” W). water temperature was recorded throughout this time. Because N. emarginata spawn throughout in July 1980 and July 1982, and (2) Barkley Sound, Vancouver Island, British Columbia (two the year. and because ambient sea water temperature varied seasonally in the laboratory, the effect sites: Wizard Island 48°51’30” N, 125°09’33” W; Cape Beale 48°47’05” N, 125°12’54” W), in of temperature on rate of development and time to maturity could be assessed. In addition, August 1980 and July 1982. All snails from subsequent years were reared as successive genera because genetic studies were being conducted on snails from geographically widespread popula tions from these initial collections. tions, I could test for temperature compensation in these traits. Finally, because snails were reared Snails were reared following the general protocol outlined in Palmer (1985b). In brief, snails from laying to maturity in the laboratory, the prejuvenile period as a fraction of total time to were sexed based on relative penis size, and single pairs of snails were placed in individual cages maturity could be computed. To place these values in context, I compared development rate, the and provided with their preferred prey (Palmer, 1984b), the barnacle Balanus glandula, on small temperature sensitivity of development rate, and the prejuvenile period as a fraction of the total stones. Food was replenished and cages were monitored for egg-capsules at regular intervals time to maturity, to published values for a wide variety of other organisms. (Table 15.1). Capsules were removed from the rock with fine forceps and placed in 3 cm X 3 cm plastic screen bags (2-mm mesh) with Velcro closures and suspended from fishing line in gently Methods running sea water until shortly before hatching (Table 15.1). Before they began to hatch, capsules Taxonomic Concerns were transferred to freezer containers (10 X 10 X 15 cm) with 00-p.m Nitex mesh sides that on the Pacific Coast of North The taxonomic status of “Nucella emarginata” (Deshayes, 1839) contained stones with small barnacles for food (B. 5 glandula and Chthania/us dalli, —5-mm basal America remains unsettled (Palmer et al., 1990). 1have inspected Deshayes’ syntypes. and they diam). After snails had begun to hatch, barnacles were replenished on a regular basis3 (Table 15.1). are clearly of the “southern” species. Hence the “northern” species, the focus of this chapter, When juveniles reached an adequate size, they were transferred to larger freezer container cages requires a new name. Several varietal names are eligible (Dali, 1915), but shells alone are with larger mesh and provided with larger barnacles on a regular basis (Table 15. 1). Prior to ambiguous and locality data are notoriously unreliable. More important, I have been unable to maturity, male and female offspring were assigned to separate cages based on a visual inspection inspect one of Middendorf ‘sspecimens synonymized with emarginata by Dali (1915). Until these of relative penis size. Mature progeny were monitored for the production of egg capsules and taxonomic problems can be resolved. I shall follow earlier recommendations (Palmer et al., 1990) provided with fresh barnacles at regular intervals (Table 15.1). To avoid introducing unwanted and refer to the species studied here as the northern species of N. emarginata. For convenience, I snails from the field, barnacle stones were collected only from quiet-water shores where N. have omitted northern from the frequent references to this species in the text, but in all instances I emarginata were absent. mean to refer only to the northern species. as the southern species is not found north of San Cages and egg capsules were held continuously immersed in running sea water and under a Francisco Bay (Palmer et al., 1990). natural photoperiod maintained by fluorescent lighting in the main aquarium room at the Bamfield Marine Station, British Columbia. 180 Larval Morphology and Evolution Temperature Sensitivity of Development Rate 181
Sea Water Temperature water temperature varied seasonally and annually. All cages were held under ambient condi Sea t2 tions in flow-through aquaria. Temperaturewas monitored periodically with a mercury thermome c-I in where the snails were held, usually every 2—4days but sometimes less 11 ter(± 0.1°C) the aquaria zi frequently. At least one temperature measurement was available for all but 14of the 120months of 0. detailed records. Because temperature sometimes varied by up to 1°Cover the course of each day and more so throughout the month, and because some months were sampled more intensively than others, the raw temperature data were rather noisy (Fig. 15.1). I attempted to remove the effects of short-term variability and the effects of gaps in the data by fitting a smooth curve via polynomial regression and moving averages. The final “best fit” to the regular seasonal variation was deter 1984 1985 1986 mined by eye. This best fitcurve was then used to generate the expected daily temperature for each FIGURE 1.1 Observed and smoothed (best fit) daily sea water temperatures at the Bamfield Marine Station main aquarium day of each month over the full 10 year period (Fig. 15.1). These best fit estimates of average room tor the period 1 January 1984 to 31 December 1986. temperature for a given day were probably accurate to within 0.1°C. The effect of temperature on development time was determined by computing the average temperature over the roughly 3-month period from laying to hatching for each individual clutch based on the data from the best fit curve through the relevant time interval. Because snails spawned throughout the year (see Fig. 15.2), development time could be monitored over a natural ska (N= 159) British Columbia (N- 607) range of temperature (8°—il°C).
“0 Duration of Life History Stages 11 Although key life history events (laying, hatching, and maturity) were monitored on a regular C.) 130 l0 basis, the uncertainty associated with each varied from inspection to inspection, and over the LI 20 duration of the study (Table 15.1). The estimated time and the associated uncertainty of each event 5- 95 were determined in the same fashion for each clutch (Fig. 15.3). For example, laying date was 10 estimated as the average of the date capsules were first observed and the previous date on which 8 that cage had been checked. The maximum possible error in the estimated laying date for that clutch was thus the number of days between those two dates (e.g., El, Fig. 15.3). The actual Feb/MarApr/May Jun/Jul Aug/SepOct/Nov Dec/Jan uncertainty associated with a given laying date would, of course, be half the value of El in days. FIGURE 15.2. Seasonal variation inthe frequency ofclutch initiationfor“northern”Nuce//a emarginata fromtwogeographically distant populations held continuously immersed Dates (first hatchlings observed in a cage) and maturity (firstcapsules produced by any in the laboratory: Torch Bay, Southeast Alaska, and Barkley Sound, British of hatching Columbia. Temperatures are mean monthly sea water temperature over the duration of the study mature offspring, whether in holding cages or as individual snails used in subsequent crosses) and (1982—1992). their uncertainties were estimated in the same manner (Fig. 15.3). The mean (± SE) maximum uncertainty associated with each life history event over the entire period of study was: laying, 13.0 days (±0.23, N = 591), hatching, 28.7 days (±0.56, N = 607), and maturity, 23.7 days (± 1.19, N = 279). Time to Maturity By chance the uncertainties for certain stages for some clutches were large, and for others small. To avoid introducing unnecessary errors, some observations with large uncertainties were excluded from the analyses. All analyses were restricted to clutches whose uncertainties were less than a predefined threshold: time to hatch 50 days (i.e., El + E2, Fig. 15.3), juvenile period Estimated: 60 days (E2 + E3); and total time to maturity 50 days (El + E3). The average maximum 1’ uncertainties after removing observations above these threshold levels were 30.2 days (N = 357), C 39.0 days (N = 166), and 24.6 days (N = 169)for time to hatch, juvenile period, and total time to Laying Hatching Dateof Started Started maturity, respectively. Note that these thresholds yielded maximum possible uncertainties and i° Clutch FIGURE 15,3. The procedure for estimating the duration and uncertainty of various life history stages, The horizontal line that actual uncertainties would be half of these values (see preceding paragraph). Sample sizes indicates time moving from left to right for an individualclutch. Vertical arrows below the line indicate actual dates, whereas those above it indicate varied for the estimates of different life history events and stages because reliable dates for all estimated dates. El, E2, E3 the maximum error or uncertainty associated with the analyses. estimated dates used in three events (laying, hatching, and maturity) were not available for all clutches. 182 Larval Morphology and Evolution Temperature Sensitivity of Development Rate 183 Time to hatch as a fraction of total time to maturity was computed separately for each clutch l60 for which both time to hatch andjuvenile period were available. The average value was computed 1401 . @hco1unbia as the average for all clutches each • : • from of the two geographic regions. :::: Comparisons with Other Species : To place the results obtained for Nucella einarginara in context, similar data were obtained from . • ••. •II• the literature for other species. Where data on time to hatch orjuvenile period were expressed as a 1 • • range of values at a given temperature, I used only the minimum for each. If data were given for a 160 range of temperatures, I estimated time to maturity only for one temperature near the Thormal” 140 temperature range experienced by the species. Where graphical data were available describing the dependence of time to hatch on temperature, these data were digitized from the published figures 120 and used to compute Q10 values. 100 Q10 Computations 80 . . 0Q values were computed from the slope (A)of the least-squares linear regression: X = tempera ture (°C), Y = log(1/days to hatch). Hence, for a given species Q10 = 10(b0’A).Least-squares linear regression seemed more appropriate here than reduced major axis regression (LaBarbera, 1989)because errors in the estimate of time to hatch were probably considerably larger than those •• • for temperature. • I • With two exceptions, Q10 values for time to hatch were estimated using all the available data published for a species. First, where data departed significantly from a linear relationship of log(1/days to hatch) versus temperature at extreme high temperature, observations near the I. 7.5 8 8.5 stressful limits were not included. Second, for one species of snail upon which several studies had 9 9.5 10 10.5 11 11.5 Seawater Temperature(°C) been conducted (Urosalpinx cinerea), one author’s results differed from all the others and were FIGURE 154. Time to hatch as a function of seawater temperature in excluded laboratory-reared northern” Nucella emarginata from (see Spight, 1975). two geographically distant populations, and in hybrid crosses between them. Only development times with uncertainties 50 days were included (see “Duration of Life History Stages” in Methods). Lines correspond to least-squares linear equations (slope SE., intercept regression ± S.E.): BC, —16.3± 1 Statistical analyses 1.40,262.5 ± .16(N = 203,r= 0.634); hybrids, —8.2± 5,26, 179.0 ± 2.55(N 32, r — 0.272);AK, —9.5 1.91,188.5 ± 1 .62(N = 81,r 0488). The slopes for BC and AKdiffered significantlyfrom Data manipulation, each other (p = .013, ANCOVA).Nofurtheranalysis was editing, and computation of uncertainties were conducted with Excel (Ver. attempted for hybrids because the data spanned too narrow a range temperature to be useful and because the of slope forthis group by itselfdid not differsignificantlyfromzero. The 3.Oa, Microsoft). Descriptive statistics, least-squares linear regressions, contingency table an here only for completeness. data are included alyses, and analysis of variance (ANOVA) were computed with Statview II (Ver. 1.03, Abacus Concepts). Analysis of covariance (ANCOVA)was conducted with SuperAnova (Ver. 1.1, Aba time to hatch increased 16.3 days for each degree drop in temperature for capsules from British cus Concepts). Columbia and 9.5 days per degree for capsules from southeast Alaska. These would correspond to an impact on development Results time per degree of approximately 16 percent and 10 percent, respec tively, of the total time to hatch at 10°C. No analyses were conducted for hybrid snails since the Although both British Columbian and southeast Alaskan populations of Nucella emarginata small sample size and limited temperature range yielded no significant association between produced egg capsules throughout the year, both spawned more frequently during the winter development time and temperature. months (December—May)when laboratory water temperatures were lowest (Fig. 15.2). Alaskan Because of the different slopes for these two regions, capsules from British Columbia took snails, however, were significantly more sensitive to seasonal cues and spawned less frequently significantly longer to hatch than those from southeast Alaska only at temperatures below about than those from British Columbia during the late summer and fall (August—November;p = .04, 10°C. For example, at 8°C British Columbian capsules took 17 percent longer to hatch than contingency table analysis). Alaskan capsules (140 versus 120 days), whereas at 10°Cthey differed by only about 5 percent (99 Over the temperature range examined (8°—l1°C),time to hatch decreased significantly with versus 94 days). The regression lines crossed at approximately 10.7°C. Because of the generally increasing temperature for capsules from both British Columbia and southeast Alaska (Fig. 15.4). inverse exponential dependence of hatching time on temperature (Johnston. 1990). these linear The effect of temperature on hatching time was significantly more pronounced for capsules from regressions cannot be extrapolated reliably to higher temperatures. the more southern region (see Fig. 15.4 legend). For British Columbian capsules, the 10 for Average juvenile period Q did not differ significantly between British Columbian and southeast development rate (1/time to hatch) was 4.93 (± 1.05 SE) whereas for those from southeast Alaska Alaskan populations (p = .80, one-way ANOVA).For both. thejuvenile period in the the was laboratory Q10 2.63 (±0.69, see Table 15.2). Based on the slopes of the regressions in Figure 15.4, was approximately 430 days (Table 15.3). Similarly, the average time to maturity, measured as the 184 Larval Morphology and Evolution Temperature Sensitivity of Development Rate 185 Table 15.2. 0Q values of rate of development (1/time to hatch) for selected fish and invertebrates Table 15.2. Continued Temperatures tested Temperatures tested (°C) CC) Species Mm. Species N” Max. Mean ’Q10 Source N” Mm. Max. Mean bQ10 Source Teleost fishes Lepadomorph barnacle Clupea harengus (Ati herring) 9 5.3 14.2 9.0 4.18 Johnston. 1990 Lepas anatifera 2 19.7 24.8 22.2 3.05 Patel and Crisp. 1960 Cvprinodon macutaris (pupfish)c 19 15.0 28.4 22.6 3.72 Kinne, 1963 Balanomorph barnacles Enchelvopus cimbrius (rockling) 12 5.3 23.1 13.4 2.80 Johnston. 1990 Balanus amphitrite’ 5 17.6 31.7 24.2 1.91 Patel and Crisp. 1960 Gadus macrocephalus (Pac. cod) 11 2.5 13.2 7.4 4.18 Johnston, 1990 B. balanus 4 3.1 13.1 7.8 3.15 Patel and Crisp, 1960 G. morhua (Atl. cod) 9 —1.0 14 6.8 2.84 Kinne. 1963 B. crenatus’ 5 3.1 18.1 10.3 2.92 Patel and Crisp, 1960 Harpagifer spp. 8 —0.4 0.6 0.1 3.89 Johnston, 1990 B. petforatus 7 9.1 27.4 19.9 2.56 Patel and Crisp, 1960 Morone sa.xatilis (striped bass) 8 15.3 22.5 18.8 3.61 Johnston. 1990 Chthwnalus stellatus’ 5 9.1 27.8 18.6 2.17 Patel and Crisp. 1960 Mugil cephalus (grey mullet) 11 10.4 29.1 19.4 2.15 1990 Elminius modestusc Johnston. 5 3.1 18.0 10.3 4.13 Patel and Crisp. 1960 Osmerus eperlanus (smelt) 11 4.9 17.8 10.3 5.77 1990 Semibalanus Johnston. balanoides 5 3.0 13.9 8.9 1.31 Patel and Crisp, 1960 Pleuronectes platessa (plaice) 11 2.4 14.3 7.7 3.06 Johnston, 1990 Verruca stroe,nla’ 6 3.0 18.1 10.8 2.99 Patel and Crisp. 1960 Scomber scombrus (mackerel) 10 10.3 21 15.5 3.77 Johnston, 1990 Echinoid echinoderms Prosobranch gastropods Sterechinusneumayeri 4 —1.9 —0.1 —0.8 9.58 Boschetal., 1987 Eupleura caudata 13 21.1 26.6 24.9 MacKenzie, 2.89 1961 Strongylocentrotus droebachiensis 4 0.0 9.4 5.4 3.12 Bosch et al., 1987 Ilyanassa obsoleta 7 11.0 28.2 20.0 2.81 Scheltema, 1967 S. franciscanus 2 10.2 12.7 11.5 2.13 Bosch et al., 1987 Urosalpinx cinerea 12 10.2 29.7 19.1 1.71 Spight, 1975 “N sample size. Nucella emarginata, AK 81 8.1 11.3 10.0 2.63 This study 10bQ = l0(b0> 186 Larval Morphology and Evolution Temperature Sensitivity of Development Rate 187 ture compensation has been noted as lacking (barnacles. echinoids, and fishes) all have pelagic LI Fish LI Barnacles B N. emarginara larval stages. LI Echinoids LI Copepods E Other Prosobranchs Questions persist about the proper analysis of temperature dependence of physiological processes (see the appendix in McLaren, 1963). For example, McLaren reports evidence of temperature compensation in rates of development of copepods both within (McLaren, 1966) and among species (McLaren et al., 1969) when using a different analytical approach that attempts to 4 circumvent some of the inadequacies of conventional Q10 analyses. Hence the apparent lack of temperature compensation in rates of development reported by some may in part reflect a poor z 2 choice of analysis. Q10 Values for Rate of Development in Northern Nucella eniarginata and Other Taxa 2 3 4 5 Not only did Alaskan populations of N. emarginata develop more rapidly at temperatures less Qof10 Rate of Development (1/days to hatch) FIGURE 15.5. Temperature sensitivity than 10°C (Fig. 15.4), but their rate of development was less sensitive to temperature variation of rate of development for a variety of marine organisms (see Table 15.2 for detailed data). The two values for N. emarginata correspond to separate estimates for than British Columbian snails over the temperature range examined (8°—i1°C, Table 15.2). This the BritishColombian and Alaskan populations. difference in temperature sensitivity may have been due to the relative differences between lab and field sea water temperatures for these two populations. For British Columbia snails, although the range of monthly mean temperatures experienced in the laboratory was less than half that of 6 surface sea water at nearby Cape Beale for the period November 1982to August 1988 (laboratory LI Echinoderms LI Bivalves LI Barnacles LI Opisthobranchs range = 3.4°C [min.= 8.0, max. = 11.4] versus Beale range 7.6°C [mm. = 6.6, max. = 5 Copepods B N. ernarginata 14.21),the mean temperature experienced in the laboratory was 0.6°C less than that of surface sea 4 LI Chitons B OtherProsobrobranchs water at Cape Beale over the same time period (9.9°C ± 0.11 SE versus 10.5°C ± 0.26, N = 70). For Alaskan the snails, mean laboratory sea water temperature was likely higher than those 3 experienced in the field. Unfortunately, because I did not manipulate temperatures experimentally to try to mimic those experienced in air (i.e., up to 25°C during the summer months), I cannot be certain whether the rates of development of British Columbian snails would be faster than (as z implied by the regressions of Fig. 15.4), or the same as, those for Alaskan snails at temperatures above 11°C. li iI. <2.5 5 10 15 20 25 30 The values reported here for rate of development to 30 Q10 (1/time hatch) were comparable to i of Time to Maturity Spent as Larva those determined from a casual survey of published values for other marine taxa (Table 15.2, Fig. FIGURE 15.6. Percentage of time to maturity (see Fig. 15.3 fordefinition)spent as larvae or “prejuvenile’for a variety of marine organisms (see Table 15,4 for detailed data), 15.5). At a 10 of 2.6, rates of development ofAlaskanN. emarginata were close to those of the The two values for N. emarginata correspond to separate estimates for the British Q Columbian and Alaskan populations. majority of other species, which exhibited 0Q values in the range of 2 to 3. The Q10 of 4.9 for British Columbian snails seemed rather high in comparison since only two other species, one fish and one echinoid (Table 15.2), exhibited higher values for rate of development. Although 0Q Q10 emarginata compared to P. sibogae (430 versus 21 d). In further contrast to these results for N values have been noted to increase at lower temperature in other taxa (Bosch et al., 1987), this is in emarginata, Huntley and Lopez (1992) report dramatic effects of temperature on generation time part an artifact of analyses. Even for chemical reactions that behave precisely according to 0Q (fertilization to maturity) in a broad survey of copepod growth: more than 90 percent of the Arrhenius’ function, is expected to increase with decreasing temperature (Schmidt-Nielsen, variance in growth rate Q10 of thirty-three species over a temperature range from — 1.7° to 30.7°C 1979: 537). could be accounted for by temperature alone. When compared to a selection of published values for other marine invertebrates, the time to Juvenile Period and Time to Maturity in Northern Nucella emarginata and Other Taxa hatch as a fraction of the total time to maturity for N. ernarginata seemed high (Table 15.4, Fig. In spite of significant differences in the rate of development reported above at temperatures less 15.6). This difference was apparent even though the prejuvenile period included time in the than 10°C,differences were not apparent in eitherjuvenile period or total time to maturity between plankton for species with a pelagic stage. First, only six of thirty-one other species spent a longer British Columbian and Alaskan snails (Table 15.3). Hence, differences in time to hatch over the fraction of their time to maturity as a larvae, and of these three were short-lived opisthobranch majority of temperatures experienced in the laboratory did not translate into a longer overall time gastropods (time to maturity less than two months) and one was a short-lived balanomorph to maturity as, for example, reported for the nudibranch Phestilla sibogae with an increase in the barnacle (time to maturity approximately three months). Second, of the eight species of meso- and larval period (Miller and Hadfield, 1990). In part this may be due to the cumulative effects of many neogastropods for which I could find comparable data, N. emarginata spent at least half again as small uncertainties affecting laboratory growth during the relatively long juvenile period for N. long in the prejuvenile period compared to the next most similar species, Strombus costatus (17.7 Table 15.4. Time to juvenile, juvenile period, and time to maturity for selected marine invertebrates Time to juvenile Time to juvenile Juvenile period Lay to Hatch to Lay to Temp. Ref.” as % of time Taxon hatch (d) juvenile (d) juvenile (d) (°C) (days) Ref. b to maturity Annelida Polychaeta Pseudopolydora kempi japonica 4 15 19 ? (13) 21 (13) 47.5 Mollusca Gastropoda Prosobranchia Mesogastropoda Polinices lewisi 42 43 (1) 915 (1) 4.5 Strombus costatus 6 36 42 27 (2) 300 (2) 12.3 S. gigas 4.5 27 31.5 28 (2) 1095 (2) 2.8 Neogastropoda Conus pennaceus 25 0 25 25 (9) 730 (10) 3.3 C. quercinus 15.5 30 45.5 25 (9) 2555 (10) 1.7 Eupleura caudata 18 0 18 25 (6) 710 (6) 2.5 Nucelta canaliculata 90 0 90 ? (12) 915 (11) 9.0 N. emarginata “northern”, BC 100.5 0 100.5 9.9 (15) 429 (15) 19.0 N. emarginata “northern”, AK 93.7 0 93.7 9.9 (15) 434 (15) 17.7 N. lamellosa 67 0 67 ? (13) 1460 (11) 4.4 Opisthobranchia Nudibranchia Archidoris pseudoargus 9 37 10 (14) 730 (14) 4.8 Doridella obscura 9 9 25 (14) 26 (14) 25.7 D. steinbergae 9 9 25 14 (14) 24.5 (14) 50.5 Onchidoris bilamellata 9 9 53 10 (14) 270 (14) 16.4 0. muricata ? ? 58 10 (14) 270 (14) 17.7 Phestilla melanobranchia ? 8 23 (14) 135 (14) 5.6 P. sibogae 5 7 12 23 (8) 21 (8) 36.4 Tritonia hombergi ? 1.5 9 (14) 730 (14) 0.2 Adalaria proxima 7 7 2 9 (14) 300 (14) 0.7 Polyplacophora Katharina tunicata 7 14 (13) 730 (13) 0.9 Lepidochitona fernaldi 12 2 14 10 (13) 182 (13) 7.1 Mopalia muscosa 10.5 11.5 15 (13) 730 (13) 1.6 Bivalvia Heterodonta Bankia setacea 9 28 14 (13) 120 (13) 18.9 Panope abrupta 18 17 (13) 1275 (13) 1.4 Tapes philippinarum 24 15 (13) 365 (13) 6.2 Tresus capax 26 10 (13) 1095 (13) Arthropoda 2.3 Crustacea Copepoda Acartia clausi 8.2 7 8.2 5.2 (7) 31 (4)@10°C 20.9 A. tonsa 3.3 7 3.3 16 (7) 16 (4)@16°C 17.1 Calanus finmarchicus 2.4 2.4 9.9 (7) 45.2 (4)@10°C 5.1 C. glacialis 4.3 ? 4.3 2.6 (7) 180 (4)@1.5°C 2.3 C. hyperboreas 6.64 7 6.64 0.0 (7) 185 (4)@0°C 3.5 Centropages furcatus 1.4 7 1.4 22 (7) 19.3” (4)@15°C 6.8 Eurytemora hurundoides 7.81 7 7.81 3 (7) 75.1 (4)@2°C 9.4 Pseudocalanus minutus 5.8 7 5.8 5.9 (7) 47.5 (4)@6.6°C 10.9 Temora Iongicornis 2.31 7 2.31 12 (7) 26.3 (4)@12°C 8.1 Cirripedia Lepadomorpha Pollicipes polymerus 25.4 30 55.4 14 (13) 365 (13) 13.2 VV VV V V U *. bV. V V U VVcVVUVUUV4VVV. V C.) £ >- — - - - cC — cr-too --C oCloe. - - c — * — C . .ctf R 1) -. . - cID C ‘ - . . . fundamental dependence only filled exhibit possibility hence do temperature hatchling acting pelagic dence what 15.7a), and obranch cean unusually l5.7c). to gastropods (Fig. predicted expanded Spight with Is particular among lite and little limit hatching period this have percent with Development hatch Taken Alternatively, molluscs constraint. When or triangles Strathmann, period Some gastropods is These Direct time 15.7). the impact to during across much ion (1975) All striking constraints constraints stage would taxa do gastropods versus at snail. rate together, for to with search precise taxa. of compared of diffusion, are caution of with dependence level were a The data Development? less maturity generally may species. development muricaceans. on development, the following to these of given unusual was still reasonable about A 12.3 results the filled precise take the intracapsular More in of suggest two later 1989). dependence Richard have more the on be imposed the should direct-developing the taxa relatively generally time temperature percent at years across among direct-developing in circles approximately Because the unusually stages take in Tightly first literature of a temperature arisen of Whether their exhibit N. systematic two that given spent this rate accuracy be rates, development (Spight However, Strathmann longer to at emarginata the by the in of respects. exercised of short intracapsular expanded take although observe development, which of due of Constrained this temperature in Fig. encapsulation capsule a total development, suggest suggests long longest time than these pronounced development the than longer and juvenile to survey precision simply dependence 15.7a), species time 14 other muricacean time egg to a many that First, constraints barnacles, Emlen, when natural has search muricaceans compared rate wall nonrandom percent. that times hatch this to capsule. to to would hatching prosobranchs by period in period suggested (Fig. which as relative in the hatch hatch, other with remains maturity: interpreting is is effect Muricacean and knowing further to on during direct-developing suggested 1976), selection in largely rate even of Temperature develop gastropods, echinoid be 15. pelagic temperature. are direct-developing to of more than development (compare suggests marine This coupled of of time to selection required 7a), is N. other to related greater suggest the the development to the temperature Table the true opisthobranch taxonomic emarginata be implies to has with for not fraction for me Figure of transformation total Gastropods echinoderms, precision organisms. meso- do seen. across with that prosobranch to meso- gelatinous Sensitivity only been 15.4). solid that than even to that encapsulated of with time rates than encapsulation that reject the muricaceans 15.6 modes of and direct-developing do the an hatch. that able though affinity versus on and variation Some is to in of time rather species of substantial do direct-developing even constrained since maturity, seemingly neogastropods, rate gastropods the this gas Second, of for this to egg neogastropods muricaceans of and spent I from Development gastropods, laboratory. of egg open broader reduce exchange, precise and of possibility. cannot muricaceans direct temperature development apparent masses would teleost this in development, may per size, in temperature. a they they constraints the circles difference the development more at the (Fig. temperature rule se range have (Strathmann seem number fishes muricacean some stage, take prejuvenile differences (compare exhibit is or But time but it Rate out could murica not precise metabo- in 15. depen less has with of into longer within even to very pros (Fig. Fig. this and 7b), the from taxa may but may of An had be to an be 191 a a if Fr j A7245. supported anonymous Marine indebted maintaining My tion Acknowledgments tially fish embryos opisthobrarich temperatures; barnacles emarginata planktonic: gastropods, FIGURE 192 (Eleven warmest and among Larval 15.7. Station (Twelve energy some per to H x 0 .0: species (this (b) C 0: by for Time reviewer gastropods Robin various Morphology the thanks capsule, 100 these 100 100 study); fraction National others 10 10 10 species I -5 to for IKinne, to laboratory cEchinoid • ACephalopod o . A A o • X initiate hatch molluscs, Mollusc Boal, species. data Opisthobranch Prosobranch Other N. Other Other Other their prosobranch D of go for [Patel + (Twenty-three emarrznala, the 1963; 0 nurse N • (in Sciences are to Murjcacea. Prosobranchia. Muricacea, Prosobranchia. and comments patience prejuvenhle days) and Barbara 4 George and for (c) Johnston, +Fish a egg 5 crosses. Evolution only higher Barnacle Crisp, coordinate as AK&BC gastropods •I planktonic direct a a to and A species .iI. single Shinn, Temperature •Copepod marine function period 10 1960: and Bunting, planktonic direct on 19901), embryo t , Engineering Thanks the temperature. assistance Hines, A spent [Spight. (Fourteen taxa. 15 A this of and ..• Steve manuscript. A water A ratio, For and copepods in 1978]), conference (°C) also the 1975: 20 0 some 0 Stricker. temperature . o species Jeanne Direct: plankton. over and + Research ochinoid •_. to Todd, species, (Eleven 25 •• a • As ++ egg Dick entire [MacKenzie, .. this .. A a in and 1991 •• Ferris A p. Compiled 0 A always, for . echinoderms A capsule + development honor 30 species prolonged prejuvenile a • l) Strathmann, Council Herb variety A cephalopods for h) from c) 35 a) of 1961; [McLaren I Wilson morphology thank their of Chris (Seven period several marine time of Scheltema, study. Canada care the was et (one Reed. Herb spent species for organisms: sources: al., staff measured having species This in 1969]). within all 1967; Wilson, I [Bosch monitoring operating at am ‘northern” vary research the the (a) (Spight, Spight, over the also et egg prosobranch Bamfield substan al., inspira a and deeply capsule; range Nuce!Ia grant 19751). 19751); 1987]), was and an of Patel, Palmer, Palmer, Miller. McLaren. McLaren, MacKenzie, LaBarbera, Johnston, Kinne. Hurley, Huntley, Hines, Grahame, Emlet, Dehnel, Cossins, Dali, Bernard. Brownell, Bosch, Literature Physiol. evidence 699—705. in foraging (Prosobranchia, marine arctic migration. Virginia. 97—117. Mar. Oceanogr. global Ann. egg. 154: America B., S. Research Bull. seasonal W. populations 1985b. 1985a. S. I 1966. A. 0. A. A. R. 984b. A. pugilus I., P. M. E., H. and A. I. I. I. 262—281. F. Biol. Echinoderm H. to J., R. B., 1963. Rev. C. R., M. W. 173: A. mollusc. K. synthesis. A. A., C. A. Zool. 1915. R., models. the Cited and R. for E., Predicting and 1978. Genetic l984a. D. Quantum Ecology 1973. Prey L. and abundance L. N. 1990. A. 1955. L. Board Can. S. 1963. Ann. C. 18: 23: in 1967. 126—135. two tropics. The and M. and J. G. R. 1989. J. 1977. Beauchamp, from 33: C. Los adjacent Notes J. 386—393. Reproduction selection 373—398. Crisp. Fecundity Muricacea): M. G. McEdward, 1961. J. Cold cryptic Species Science K. Corkett. effects Rates M. Oecologia Rev. of Effects basis Gayron, Am. 104—119. Studies 42: Stud. Roques, Fish. Hadfield. changes Analyzing Branch. development Vancouver Bowler. Canada, Reproduction, Biol. on D. of adaptation Growth 1960. 3 1: Nat. of of regions. the of 17—338. species embryos cohesiveness G. 2: Aquat. by 248: 301—340. of and shell growth Bull. of on temperature and species 55—136. M. Venezuela. temperature in 62: Lopez. 1985. 140: thaidid and Preliminary 1987. Rates the Tech. in 1990. E. the 356—358. and body gastropod variation Island. E. three D. of Proc. 162—172. Sci. 137: acorn in J. R. rate 201—242. of and biology Reproductive Steele, reproduction northeastern of marine Zillioux. Temperature of Developmental Rpt. laboratory S. R. size 1992. gastropods: gastropods 20: 486—493. species the of and U.S. larvae development Biol. barnacle Woodruff. Strathmann. and Bull. as copepod in on 42: 685—727. molluscan shell results. and of organisms. genetic Temperature-dependent a Thais salinity growth Nat. factor Bull. 1969. 1—41. of of the Mar. morphology J. culture, intertidal Balanus of the Pacific as patterns biology Some Mus. emarginata naticid S. Temperature Malacologia eggs. control 1990. the 169: a in Temperature Sci. arrest of on Antarctic subgenus Pearse. of 1987. function ecology Philos. oyster zooplankton, 49: marine the and Nucella. observational 638—651. 27: Biol. pacificus of of clam Reproductive, barnacles during of Echinoderm 557—572. embryos marine need growth 668—680. shell 1987. drill (Prosobranchia, Trans. of Nucella and Bull. sea drill and 25: Sensitivity adaptations larval latitude. Veliger not Eupleura evolution. color urchin Pilsbry: 477—491. invertebrates. brackish Development, from production of Polinices 131: and Roy. of reflect Chapman and inhabiting Stroinbus life larval several and the morphological, central 457—469. 33: Sterechinus Physiol. Soc. experimental and A of caudata speciation. form water adaptive of Ann. 325—338. fugitive lewisi ecology Development Muricacea). life-span Lond. copepod of & species California. gigas, the Oceanogr. in Hall, marine Rev. metamorphosis, animals. Zool. Thais in (Gould). northwest B species. value neumaveri. viewed the Ecol. 326: S. Evolution of extension eggs London. field 28: and emarginata copepods: York costatus I. barnacles. of Biol. Oceanogr. Mar. 655—667. Rate Banding 115—143. from Syst. Fisheries genetic tests Limnol. from vertical coast River, Bull. Biol. Biol. 39: in the 20: and of and 193 the a of a 194 Larval Morphology and Evolution Perron, F. E. 1981a. The partitioning of reproductiveenergy betweenova and protective capsules in marine gastropods of the genus Conus. Am. Nat. 118: 110—118. 16 Current Knowledge of Reproductive Biology in Two Taxa of 1981b. Larval biology of six species of the genus Conus (Gastropoda:Toxoglossa)in Hawaii, USA. Mar. Biol. 61: 215—220. Interstitial Molluscs (Class Gastropoda: Order Acochlidiacea 1986.Life history consequencesof differenceindevelopmentalmodeamonggastropodsof the genus Conus. Bull. Mar. Sci. 39: 485—497. and Class Aplacophora: Order Neomeniomorpha) Scheltema, R. S. 1967. The relationship of temperature to the larval development of Nassarius obsoletus (Gastropoda). Biol. Bull. 132: 253—265. Schmidt-Nielsen, K. 1979. Animal Physiology.Cambridge University Press, New York. Spight, T. M. 1975.Factorsextendinggastropodembryonicdevelopmentandtheir selectivecost. Oecologia 21: 1—16. M. Patricia Morse 1976. Ecology of hatching size for marine snails. Oecologia 24: 283—294. Spight, T. M., and J. M. Emlen. 1976. Clutch sizes of two marine snails with a changing food supply. Ecology 57: 1162—1178. Strathmann, M. F. 1987. Reproduction and Developmentof Marine Invertebrates of the Northern Pacific ABSTRACT Two taxa are important members of the molluscan assemblage in the interstitial Coast, University of WashingtonPress, Seattle, 670 pp. environment, the well-represented gastropod order Acochlidiacea and the lesser known Strathmann, R. R., and M. F. Strathmann. 1989. Evolutionary opportunities and constraints demonstrated aplacophoran family, Meiomeniidae. Adaptations of the reproductive systems, discussed for by artificial gelatinous egg masses. In J. S. Ryland and P. A. Tyler, ed. Reproduction, Genetics and representatives of these taxa, are consistent with a general reduction in the organ systems Distributions of Marine Organisms. Olsen & Olsen, Fredensborg, Denmark, pp. 201—209. associated with minute species of molluscs. Inthe acochlidiaceans, four out of five families are Todd,C. D. 1991.Larval strategiesof nudibranchmolluscs:Similarmeansto the sameend? Malacologia32: interstitial; two of the families are composed of monoecious species and one of dioecious 273—289. species. Spermatophores have evolved for sperm transfer with a subsequent reduction in accessory copulatory organs. In mature females, only a few large vitellogenic eggs are present at any one time, and where known, egg capsules with few developing embryos enclosed are reported. The aplacophorans, represented by the family Meiomeniidae, are monoecious, with small numbers of vitellogenic eggs and copulatory spicules. Introduction Adaptations have evolved for interstitial molluscs, ranging from 0.5 mm to 3.0 mm in length, to live in the pore spaces of sediments. Such adaptations are evident among representatives of the gastropod order Acochlidiacea and the aplacophoran order Neomeniomorpha, which constitute a major part of the molluscan assemblage characteristic of coarse sand habitats (Morse, 1987). These molluscs are cosmopolitan in distribution, occurring in subtidal and low intertidal habitats in both temperate and tropical waters. The reproductive biology of these interstitial species is poorly known. Swedmark (1959, 1964) was the first to consider adaptations of organisms living in the interstitial environment. He investigated the biological adaptations of interstitial molluscs and noted that they possess a small number of reproductive cells, reduced organ systems, and a tendency for encapsulated development of the larvae (Swedmark, 1968a). Acochlidiaceans are shell-less opisthobranch gastropods, arranged in five families, Micro hedylidae (Unela, Microhedyle), Asperspinidae (Asperspina), Ganitidae (Ganitis, Paraganitis), Hedylopsidae, (Hedylopsis, Pseudunela), and Acochlidiidae (Acochlidium and Strubellia) (Ar naud et al., 1986). The first four families of acochlidiaceans are minute (0.5 mm to 3 mm in length) and are known only from the interstitial environment. Members of the family Acoch lidiidae are larger (30 mm in length) and are found mainly on Pacific Islands in freshwater streams where they live under rocks (Rankin, 1979). An interstitial freshwater form from the Caribbean M. Patricia Morse, Marine Science Center and Biology Department, Northeastern University, Nahant, MA 01908. 195 Waterville, W. Stephen George Edited The Division Department State Department New Development Marine Baltimore Reproduction Herbert Johns Mexico, University, by of L. A. and Science, Maine Shinn Wilson, Hopkins Stricker of of Albuquerque, Invertebrates Biology, Biology, London Kirksville, Northeast Jr. University Colby University of Missouri and New College, Missouri Mexico Press of