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Dissertations, Theses, and Masters Projects Theses, Dissertations, & Master Projects
1958
Growth and Reproduction of Eupleura caudata (Say) in the York River, Virginia
Clyde L. MacKenzie College of William and Mary - Virginia Institute of Marine Science
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Recommended Citation MacKenzie, Clyde L., "Growth and Reproduction of Eupleura caudata (Say) in the York River, Virginia" (1958). Dissertations, Theses, and Masters Projects. Paper 1539617371. https://dx.doi.org/doi:10.25773/v5-935h-ds74
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IN THE YORK RIVER, VIRGINIA
By
Clyie L. MaeKenasie, Jr.
V irg in ia Fisheries Laboratory Gloucester Point* Virginia May 1958
A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE
REQUIREMENTS FOR THE DEGREE OF MASTER OF ARTS
FROM THE
COLLEGE OF WILLIAM AND MARY
'Obra* ^
OF THE VIRGINIA FISHERIES if&ORATOfU ACKNOWLEDGMENT!
The writer wishes to- express his deep appreciation to Dr.
William Jf* Hargis, Jr. lor suggesting the problem and lor his personal guidance throughout the course of study. Thanks to Dr*
Willis G. He watt, who identified most of the invertebrates; to Dr*
J*. I*. McHugh lor his many Suggestions; to Mr. Robert S* Bailey lor taking such excellent photographs; to Mr. Dexter S.* Haven and
Mr* Curtis S* Leigh lor aid .in. collecting' samples; to Dr* Jay D,
Andrews and Mr* Willard A. Van Engel for valuable criticism of the manuscript; to Dr. Sewell H* Hopkins for supplying useful literature; to Miss Patricia ft* Conner for typing the manuscript; and to the rest of the staff and fellow students of the Virginia
F is h e r ie s Laboratory for their suggestions and wholehearted .+ cooperation, TAB&ft OF CONTENTS P age INTRODUCTION »*-*»***.«»•«*«*«•'*»•, I
MATERIALS AND METHODS * * * ...... 3
GROWTH * * * + .***«»«**#*. J * * », « *-> ... f
Pattern of growth 4 * * * **#.»♦**.♦*...* f
leeogaiitos* of year classes *♦#♦*«**♦*»*** ♦ to
Cessation. of growth at sexual maturity*•«*••*•«* 19
REPRODUCTION # * * ...... z\
Age and length at sexual maturity » * * • * ...... t l . Sex ratio * ♦****##•♦******♦»•■*■*• 24
Evidence against sex reversal ***♦••■♦****** 2?
Copatattoa zs Overwintering of sperm&toeea In females « .*•*♦#. i t
Seasonal activity . 41
Spawning period *- * * * * * • ♦«••♦***•»«.* 4 4
Intensity and duration of ovlposition * # * * ♦' ♦ * * * * 49
Biim of egg~ea#e is,position«*•*»»*»•♦»•*« 16
Description of cases and embryos *********** $S
Numbers of embryos per case • ******* _* * « * *' 63
Incubation period .*.*••..*.•*..*...• 6 8
Percentage of embryo#reaching protoconchstage * * * * f I
Predators and associates of egg cases * * ...... f Z
SUMMARY AND CONCLUSIONS ******** ft
LITERATURE CITED* • * * ...... * * 81 Mtmw * wJ? M tiwWmmw P#gt 1 Map of IfofB Blror atiowitig «xp»rlm*t&t«l a t as arnd collect tloa aitat * * * * * **»»#»««• * ****** . * 4
Z £xpt*t«noiitalmgm mm& la loli drM* * * * * * * * * * * 4
I Inaid# of c#g«****** * • **•«•*•«*»*♦• 4 4 i**ngih~fr«cju#m:ie» of ifilU la moolMy It&p catch*# * . . II
§ Drill# of &g#»groups 0, |f and***..**« 114- * * * * 15
4 Trap c**ct* «on#d hy $h«ii ehataolafa into age group# I and II* * * * * * * ****** * * * * . If T Copul&tory attitude of &. caudata • Sf
i T wo maloi copulatiag with otic famal#********** 2 f
f Seasonal pattern# temperature* copulation* and spawning $5
10 Seasonal pattern# of' temperate?#* boring* it#$ catch##* copulation and apsmlog la If if * #•***#«*«* ♦ 35
11 Drawing# of egg caret**************** i f
U5T OF TABUBS
I Accuracy of otieerrer# la •opatoiteg ag# group# * * * * * 15
1 lengths of ovipositing female® * .* ****♦**.,♦** 23
3 Sox ratio# of drill#in 1955 . **♦'*.* . * * * * * . 25
4 Sox ratio# of drill# to Ifif * «***•******«* 25
5 l*#ngth~fre$uettcy copulating individual#******* 33
5 Ovipredaciioa of female* isolated from mala# ***** 39
f segueac# of eopoletery# boring, nod spawning activi ty of individual drill# ******** .* * * * * * « • • • 42 $ Buration and intensity oi spawning by individual caged !« m a l« «...... * . . SI
9 Comparison of oviproductlon in successive years by individual females . § 2
10 Numbers of agg casas par cluster in cagas and on shalls in experimental araa . * , * ...... $3
11 Substrata dj, caadala agg casas §7
12 Relationship of shall length of females to langth of casas 61
13 Number* of ambryos par case in various sambas . • 64
14 Variation in number of ambryos par casa dapositad by savarai lamalas ...... 6 ?
15 Variation in number of ambryos par casa dapositad by a single female in Table 14 * ...... * . • 6 ?
16 Incubation period of K, caudate e m b r y o s ...... 70
17 numbers of damaged and undamaged agg cases collected in experimental area 73
1$ List of plants and animals observed on agg casas * . 75 INTRODUCTION
Eupleura caudata (Say) (Order Neogastropoda: Family Muricidae),
the thick-lipped or rough oyster drill, is a close relative of the smooth
drill, Urosalpinx cinerea (Say), which occurs within the same geographical
range along the shores of the Atlantic coast from Massachusetts to the
eastern coast of Florida. Both species are well-known predators of
oysters and perhaps other commercially valuable bivalves. Except in
isolated localities, U. cinerea is the dominant species, and as a result
has received more scientific attention. Until Haskin (1935) showed that
E. caudata females deposit more embryos per case than U. cinerea in
Barnegat Bay and noted the differently-shaped egg cases, the only
publicised differences between the two species lay in the morphology of
the shell. Though the species is present in some numbers, McHugh (1956)
did not find a single E. caudata among hundreds of drills collected from
pier pilings in the vicinity of Gloucester Point, and we found only one in
our large samples. This suggests that the two species have different
vertical distributions. Haskin (1935) and Galtsoff, Prytherch and Engel
(1937) stated that the two species do not differ in their destructiveness of
oysters. Stauber (1943) observed copulation of a single pair and stated
that numbers of egg cases deposited by caged females vary from year to
year. Engle (1935) and Andrews (1954) briefly described spawning patterns for a single year. Other than the fact that certain workers (See Carriker,
1955) believe the ratio of E. caudata to U. cinerea is increasing in some ■2 « localities, little else is known about the natural history of this animal.
This study was undertaken to elucidate certain aspects of growth,
reproduction, end ecology of B* caudata in the eelgrass sone of the York
River to acquire basic information which might be used in controlling this pest. - 3 - MATERIALS AND METHODS
Description of the area
All drills studied were taken in the vicinity of the Virginia
Fisheries Laboratory at Gloucester Point, Virginia, six miles from the mouth of the York River {Fig. 1). This area is estuarine with salinities varying between 14 and 22 parts per thousand except during severe droughts and freshets. Oyster drills and several other snails live within the eelgrass zone, a narrow strip about 50 yards wide in the experimental area, which was bounded by Marshall’s pier and the ferry pier. The grass is abundant and almost continuous. At extreme low tides the inner edge of the grass is exposed and the outer edge is rarely covered by more than five or six feet of water. The bottom slopes moderately away from shore, and because it is protected by the tip of Gloucester Point, the experimental area does not have rapid currents. Wave action disturbs the bottom only during heavy easterly winds. Within this zone, E. caudata had a mean density of 3 per square yard; whereas,tJ. cinerea had a mean density of 37 per square yard.
Several samples of egg cases weee obtained at Tillage's oyster ground located upriver from the laboratory (Fig. 1). Except where noted samples were taken from the experimental area. - 4 -
T illa g e 's O y s te r GroundlG,ouce'ster pt
York R iver Coleman Bridge
York tow n
Wormley's Rock
I MILE
Fig. 1. The York River in the vicinity of the Virginia Fisheries Laboratory showing collection sites. Inset shows experi mental area. Dotted line shows extent of eelgrass. . 5 -
Aquaria
Running-water aquaria of approximately two and seven tenths cubic feet capacity were employed to make close observations of copulation. River water from the end of the laboratory pier was con tinuously supplied by centrifugal pumps.
C ages
Several phases of this study were conducted in cages suspended in the river along the laboratory pier one foot from the bottom, with about one to three feet of water covering them (Figs. 2 and 3). Cages consisted of wooden frames with masonite bottoms. The sides and removable top were covered with large-mesh plastic screen, four holes to an inch. Masonite dividers pryented contact between drills in adjacent co mpartments.
The cages were 37 inches long, 16 inches wide, and6 inches deep,
The number of compartments per cage varied from 2 to 12. Later models incorporated plastic screen bottoms (8 holes to an inch) which were more effective than solid bottoms of earlier models in permitting sediments to pass through. All cages were suspended in seasoned, tarred oyster trays for support and stability. Except where noted several one- and two-year-old oysters were placed in each compartment as food and were not replaced the whole summer. - 6 -
Experimental cage, oyster tray, and davit used to raise and lower the cage.
Compartments and screen bottom of cage. - 7 -
Traps
Drills and egg cases were obtained with traps or collectors
consisting of flat, 27- by 12-inch chicken-wire bags containing small oysters and often barnacles and mussels as bait. These bags were tied in the center by a rope attached to a small buoy. Drills which
moved to the oysters were collected by carefully lifting the traps and
shaking them into a shallow screening tray. Since they reduced the abundance of drills locally, traps were moved to new areas after each collection to secure as many drills as possible,
Square yard samples
To obtain accurate estimates of drill densities, a square metal caisson enclosing a square yard was placed on the bottom. The top 3 or 4 inches of bottom within was scooped into a screening tray, sifted, and sorted.
Temperature
Temperature records wereecompiled from data collected at the
0. S. Coast and Geodetic Survey sub-station located at the end of the laboratory pier. Since the cages and traps were five or more yards inshore of the temperature recorder, temperatures at cage and trap sites may have been slightly different from those at the tide station. - 8 -
Seating
The method developed by Margie (195?) to determine i«x of living snails was used* He found that oyster drills held under water would attach to 000*0 finger. By carefully rolling the shell back the presence or absence of a penis could be detected.
Measurements
AM measurements of drills, made with vernier calipers and cited in millimeters, are of the long aads of the shell from apical tip to siphonal tip, i^e., shell height or shell length. Egg cases and embryos were measured microscopically using a calibrated ocular micrometer. GROWTH
Pattern of growth
Alter the initial varix has formed, shell growth In B. caudata
usually occurs as a thin layer which begins at the inner edge of the
margin or lip and without stopping to reinforce proceeds from one varix through an arc of ISO* or one-half whorl. After flaring out to form the next varix, the animal then reinforces this thin shell by depositing
successive layers of shell on the inside. Thus thin lips are an indication of active growth. Often when mature Individuals pass the winter their thin siphonal canals are broken or eroded, During the summer they deposit enough new shell to cover the siphon but unless accompanied by lateral growth this is merely repair of damage and not actual growth.
Moor. (1936) h „ ,how« that Pu^ur.t a g ! - Th^. U ptU u. . another prosobranch muricid, has a similar growth pattern except that it does not form varices. - 10 -
Recognition of year classes
Estimation of age by length frequencies
From July to November 1956 and from May to October 1957,
lengths of drills taken in monthly trap catches were recorded, grouped
into one*millimeter intervals, and plotted as percentage frequency
polygons {Fig. 4). In July 1956, length frequencies showed what appeared
to be a 0ingle modal group with several peaks. This mode showed a
definite progression to the right with each successive month of 1956, and
is clearly represented as tie large portion of the right-hand mode each
month in 1957.
In late August 1956, five small drills appeared in trap catches and
a few more were collected in September. Of 43 collected in October, a
random group of 32 was measured and plotted along with the rest of the
catch. This modal group with a range of 5 to 14 mm was separated by more
than 3 mm from older drills. In the November 1956 sample, and in monthly
samples of 1957, the left mode corresponds with the left mode of the October
1956 sample.
It is probable that drills in the left mode in the October 1956 sample
belong to age-group0 . There are only five mm to the left of it in which to
include a younger age group and separate the two groups by more than three
mm. It would be unusual for age-group0 to be less widely separated from the 1*8 than the I's are from the H's. When first collected in late August, FREQUENCY IN PER CENT OF TOTAL TRAP CATCH IO i. . otl ta cths fE. adt i xeietl area E_. ofexperimental in catches trap caudata Monthly 4. Fig. hwn lnt feunis f g gop 0, group age of frequencies length showing 20 I + 3E+ + I 1 + 3L+ + 1 EGH N MILLIMETERS IN LENGTH - 6 AUG 56 AUG 56 6 3 SEPT 56 56 SEPT 3 8 JULY 56 56 JULY 8 8 OCT 56 56 OCT 8 14 NOV 56 56 NOV14 N-80 N-123 11 N-109 N-65 N-54 - 35 + 1 3 1 + -1 MAY 9-31 57 1-31 JULY 57 1*31 AUG 57 -0JN 57 JUNE1-30 1-15 OCT 57 1-15 57 OCT 1-30 SEPT 57 57 SEPT 1-30 1, N-616 N-1,133 N-242 N«327 n 11+. and
- 12 -
these drills were quits large, but in earlier observations of U. cinerea
by McHugh (personal communication), suspected young-of -the- year drills
had reached a mean siae of 6 to 8 m m when they were first collected in
August and September* Apparently young-of-the* summer drills are not
available to traps until mid-summer. Growth rate of age-group 0
E. caudata on natural bottom is unknown, but conceivably may equal or
exceed that of older drills which grew from 12 to IS mm to over 20 m m
in 4 or 5 months in cages* Most caudata concha emerged from cases
during the first week of July at a length of 0. m9 m . Thus, in three months
they had grown 5 to 10 m m .
The right mode of the October 1956 sample may represent age
group 1 and older drills, 114 * The plus (4) sign is used since older age
groups cannot be separated hi this mode on the basis of length* Usually
E. caudata cease growth in the third summer and, therefore, length frequencies of age groups coalesce. Growth of the 1956 year class In 1957, now labelled age-group I, as indicated by the progression of the mode about
3 m m to the right, is believed slower than the previous year because the lower length limits of the early 1956 samples were much farther to the right than those of the 1957 samples* In 1957, drills of age-group I grew much faster in cages than on natural bottom. Slow growth on natural bottom may have been the result of intensive competition following a very large spawning in 1956 and subsequent overcrowding of the environment.
It is striking that age-group 1 drills are dominant in the catch in 1957, Such a dominance of one year claee may subsequently affect other phases
of the drill*s life history* each as strength of succeeding broods and age
at sexual maturity.
In 1957, only one recognisable individual ($.0 m m ) of age*group
0 was taken, on October 3. This apparent lack of young~of«the~year
drills may have been the result of limited spawning and hand*removal
of large numbers of egg cases from the experimental area*
Estimation of age by shell characters
Since it was apparent that shells of E. caudata erode gradually
with time, it was thought that drills could be sorted info age groups on the basis of the degree of shell erosion. Presumed age-group0 d r ills of the October 1956 sample were smaller than those caught in earlier catches, and also differed in that the embryonic shell was entire and the axial ribs
were sharply sculptured. The lack of any noticabie shell erosion further supports the contention that the drills were newly hatched. Fart or
sometimes all of the embryonic shell was eroded away during the winter of 1956*57. These drills, now called age*group I, could still be separated from older ones because the sharp apex of the spire and the chiseled appearance of the shell sculpture had not appreciably changed. Older drills, labeled age*group H+, had blunt spires and smooth ribs. Separation of these two age groups in 1956 could have been attempted if the difference in shell characters had been known. * 14 *
A summary of characters used to separate age*groups I and 114 on August 23, 1957, and age-group 0 on October 3, 1957, (Fig. 5) follows;
Age*group 0 - Apex of spire sharp, embryonic shell entire,
no visible erosion of shell, sise small;
Age-group 1 - Apex of spire sharp, remnant of embryonic
shell usually present, apical whorl less than
1 mm in width, axial ribs usually sharply
sculptured, sise moderate;
Age-group 114 * Apex of spire blunt, apical whorl 1m m or
greater in width, axial ribs blunt or short only
on last half whorl, sise large.
To test whether the differences in shell characters were distinct enough to separate drills into lots, several laboratory staff members were ashed to separate a mixed sample of age-groups 1 and H4. The sample had been sorted previously into groups marked by inserting labeled pieces of paper into the shell cavities. The characters used to separate the groups were carefully described to the experimenters, and sample drills were furnished* In each test, drills were sorted with almost 100 per cent accuracy (Table 1).
F igu re 6 shows the complete catch of August 23, 1957, grouped by shell characters into age-groups I and H4 * - 15 -
Fig. 5. Individuals (L. to R.) of age-groups 0, I, and II+. x 2.5 Tablet 1. Accuracy of observers la separating age groups, us lag defined morphological character la tic s HN| I a#
- 17 -
§ f f ff 4 $ $ t f f $ 4 44444 #4f ♦ f 044444 ^ f t H Ht+444 A f f ♦♦♦ttftt♦
Fig. 6. Photograph of a complete random trap catch (August 23, 1957) of E. caudata sorted by shell characters into age-group 11+ on the left, and age-group I drills on the right, x 0.7. - 18 -
Comparison of langth frequencies and shell characters
When drills in October and November 1956 trap catches were separated by shell characters* the frequency distribution of age*group
0 agreed closely with the left mode* and the combined age-groups1 and
H4 agreed with the right mode. In all 195? samples* the frequency distribution of age-groups1 and 114 agreed closely with the left and right modes.
Although much of this evidence is circumstantial and does not absolutely establish the ages of individuals* shell characters are probably reliable indicators of age for most drills in a sample. A reliable method to distinguish age groups offers several advantages!
( 1) growth can be traced separately for each year class* (2 ) relative strengths of year classes can be assessed* and (3) age at sexual maturity can be determined. Cessation of growth at sexual maturity
Moore (1936 end 1939) stated that T, lapilius ceases growth at sexual maturity* The following date indicate a similar pattern of growth for caudata if a female is called mature when she deposits her first egg case*
Only one of 10 females which oviposited in cages in 1936 showed evidence of growth and that individual deposited only a half-whorl. Of this group, eight survived the winter and none grew in 195?. Of seventeen other females isolated in 1956, twelve oviposited for the first time in
1957, and did not grow during the summer* Three of the five reproduc- lively inactive in 1957 showed no growth, while one grew two half-whorls, and the other one half-whorl. It thus appears that females grow little, if at all, after egg case deposition begins* Although it is difficult to deter mine sexual maturity by external criteria, males also apparently cease growth at sexual maturity. In 1956 only 10 of 30 caged males grew (length range 14*4 m m to 23. 3 mm), one two half-whorls and nine one half*whorl.
Their length range matches that of mature copulating males (Table 5),
Presumably then most of these males were mature. Of 24 of the same males carried through 1957, 22 showed no growth and only two grew a half-whorl.
Beginning June 25, 1957, a record was kept of the numbers of
E. caudata in trap catches which showed evidence of recent growth. 20 *
Only two of §22 (. 04%) age-group 114 drills showed signs of growth, while IdS of 1,108 (14. 7%) age-group 1 drills showed growth.
In testing & newly*designed drill dredge, approximately2 0 0 marked drills were scattered between the Laboratory and ferry piers on August 17, 1956. Sixteen were recaptured on traps between May 13 and July 18, 1957. Of these, eleven showed no growth, three added a complete half-whorl, one two-thirds of a half-whorl, and one one-quarter of a half-whorl during the interval. Because they were chosen according to the mesh size (four holes to one inch) of the experimental dredge, it is probable that most of the eleven were mature when released.
Another indication that growth ceases when drills reach maturity is that the right limb of the curve representing age-group 114 does not shift to the right through the growing season (Figure 4). ■* 2 1 -
MEFjtomrcTioif
A lt and length at seamal maturity
The writer early suspected that female drill* did not mature until after their second summer of III*, because in 1956 of 50 female* in c«i«« only11 largo ones deposited egg cases. yooag-ef-the-summer war* not yat hatched whan the drills war# caged* m many of tha 19 remaining war a undoubtedly In thalr second summer of Ufa. Siateen of tha If ovipositing fa mala* in cages survived tha winter af If§6-57 and tan oviposited in If ST. In another experiment, nina pairs of age* group 1 drilla (mean length 12.Z m m , range T. l*t?,t mm) war# isolated in separate compartments af a cage far tha entire summer af If ST.
Since mast drilla ware too immature ta ha eened whan the experiment was began* same of the pairs may have bean of mined sea* Also., tarn mature males (lengths 55.1 and 15.2 mm) ware paired with two age*groap
1 females (14.1 and 17.1 mm) in this cage. In addition, f l drills (mean length 10.2 mm* range 4. $*20. 5 mm) af age-.group 1 ware held together in a cage, f rom M ay 10 to July 20 this group was reduced by heavy mortalities ta IS drills. No egg cases were deposited by age-group 1 females in these three experiments though many ware deposited by other caged drills of larger sises. Ovipositing females less titan if mm ware n ever o b se rv ed . It# therefore* seem s probable that f£* caudate females are net reprodectlveiy active until after the second summer and after they have attained a else of 19 mm or mere. * 52 *
Tables 5 and 5 shew tbs extensive ?«ag« of length* of mature females. Since there is good evidence that females cease growth at sexual maturity* this probably means that there is considerable individual variation is growth and/or age at maturity sad that maturity Is attained at various lengths. The minimum length of mature E. caudate In the experimental area appears to be about If mm for females and 16 mm for m ales. * 23 *
Table 2* Sizes of females which deposited egg cases in cages or on traps*
Total length Ho. of individuals in JW 1956 1957
19.5 3 I
20.5 3 3
21.5 7 4
22.5 10 0
23.5 12 7
24.5 12 5
25.5 8 6
24.5 3 6
27.5 i 2
2 0 .5 0 3
29.5 0 0
30.5 0 0
31.5 I 0
32.5 0 ...4.. TOTAL 60 38 - 24 -
Sex ratio
Sex ratios were obtained by eexing drills collected on traps. Age
groups were not recognized in 1956; hence, sex ratios of different year
classes could not be determined. The July and August samples show a
nearly 50:50 ratio, but the samples in the three succeeding months con
tained progressively more females (Table 3), Separation of two distinct
age groups in 195? permitted sex ratios by age to be obtained. Considering
age-group 114 only, in May males were slightly in predominance, but
beginning in June a larger proportion of females came to the traps (Table 4).
The percentages of females occurring in the traps appear to follow the
seasonal cycles of copulation and spawning (Figs.9 C and 10C). It is
possible that both sexes move to shells or traps in about equal numbers
to copulate and when copulatory activity wanes and spawning begins,
larger and larger numbers of females move to shells in traps to deposit"
their cases. The samples after July 31 are probably too small to be
significant but the nearly equal numbers of sexes in the October 9 sample
may coincide with the fall copulating period. Unfortunately many age-
group 1 drills could not be sexed in 195? because they were too immature, thus their sex ratios were not determined. Sex ratios in 1956 and 195?
are unbalanced in favor of fem ales, but this may be due to selective
sampling by traps. - 25 -
Table 3. Sex ratios of 1956 trap samples (Age-group 0 not included)
Date Uncertain _ 99 do - total Per cent 99
Jul 8 8 38 37 75 50,6 Aug 6 7 34 41 75 45.3 Sep 3 4 58 46 104 55.8 Oct 8 0 25 10 35 71.4 Nov 14 0 24 6 30 80.0
ta b le 4. Sex ratios of 1957 trap samples (Age*group 11+ only)
Date Uncertain m .....m ...... total Per cent 99
May 8 1 25 39 64 39.0 May 11 0 9 27 36 25.0 May 13 0 15 29 44 34.6 May 15 0 20 23 43 46.5 May 22 0 31 33 64 48.4 Jun 5 Q 21 18 39 53.8 Jun 18 0 46 29 75 61.3 Jul 4 1 31 19 50 62.0 Jul 17 0 15 6 21 71.4 Jul 31 0 30 9 39 76.9 Aug 20 0 5 0 5 1 0 0 .0 Sep 4 0 7 6 13 53.8 Sep 26 0 5 4 9 55.5 Oct 9 0 11 13 24 45.8 Oct 25 0 4 0 4 1 0 0 .0 - 26 *
Although his collections cams from different localities at various times of the year, Cole (1942) found nearly the same pattern for dredged
U. cinersa in England. At the beginning of the summer the sea ratio was nearly SOsSO, thereafter the proportion of females increased. He felt that the dredge collected mostly drills on the raised surfaces of the bottom. .27 .
Evidence against sex reversal
Nineteen females and twenty*one males isolated on May 16, 1956 survived to August 31, 1957, sixteen months later, when they were sexed and found to have retained their sexual identities. Eight other females and seven males, isolated for times ranging from three to fourteen months, were the same sex as when isolated.
Morf&ological examination of the external reproductive organs of denuded drills and smears of gonads of over eight*hundred males and females gave no evidence of the existence of individuals with mixed sexual characteristics, i. e ., actual or potential hermaphroditic animals. Mature females possessed yellow, white, or orange gonads with large lobes con* taining vitelline bodies. Mature males possessed large penes, yellow or orange gonads with small lobes containing spermatozoa, and usually swollen vasa deferentia. If either hermophroditism or sex reversal occurs at least a few of these hundreds examined should have showed some indications of such a condition. * 28 -
Copulation
A tingle partial copulation was accidently teen by Dr. X*. A.
Stauber when a paired duet of drilla was taken from a trap and put into a laboratory aquarium for observation. Stauber (1943) reported that the
male mounted the female on the right side, formed the anterior part of bit foot into a email groove, and then extended the penis through this groove into the female's mantle cavity and, presumably, vagina. Even though distrubed, this pair copulated intermittently for 21 days.
Our observations of captive drills confirm Stauber*s observations.
Prior to the copulatory act, the female usually crawls up one of the walls of the aquarium and assumes a stationary position with her siphonal canal pointing upward and her mantle cavity exposed. The male, often seen on the female's shall when she is crawling about or on the glass nearby, contacts her and assumes the following copulatory position after she exposes her mantle cavity. He usually takes up a position on her lower right side with his siphonal tip pointing in the same direction as that of the female.
The male's foot then extends to the rim of the mantle cavity of the female and forms a groove in Its anterior and through which the penis is inserted
Into the mantle cavity. Although obscured from sight by the curve of the shell, the penis presumably enters the vagina (Fig. 7). On termination of copulation, the male withdraws the penis and moves either to another part of the female's shell or entirely away. Meanwhile, the female closes the - 29 -
Usual copulatory attitude of E. caudata in aquaria.
Copulation with penes of two males extended into mantle cavity of one female. * 30 - mantle cavity by pressing her shell to tbs substrate. Pairs war# observed in copals oa aquarium walls, on oysters on the bottom, and on the bottom of the aquarium. It is not easy to ascertain that caged drills are copulating because the female's foot is attached to the sub stratum and the male's penis cannot be seen without disturbing the pair.
As a check, pairs were carefully lifted each time they were seen in copulatory position and often the male's penis was seen retracting, but usually the male withdrew as the female retracted her foot and the intromittent organ was not regularly seen. Close observations disclosed that many males whose penes were already retracted, still retained the groove thus affirming that the pair had been copulating. Most of the lifted pairs showed either the penis or the groove. Furthermore, pairs usually separate unless they are about to resume copulation. Therefore, it is safe to conclude that most paired drills are or have recently been ha copula.
On three occasions "trios" were observed in aquaria. Each
Involved a female and male In the usual position with another male in copulatory position on the first male. Twice extended penes of both males were seen; the other time only one. Usually the male next to the female is in copula with her, while the penis of the second male extends into the mantle cavity of the first, but both males may attempt copulation with the female at one time (Fig. 8 ). Copulation between two functional males, the middle one acting as both male and female, and another female has been - 31 -
reported lor the hermaphroditic species JLymaaea st agnail a appressa
Say, but this has never been reported in dioecious gastropods (Crabbe,
1927). Inasmuch as E. caudata is not hermaphroditic, these trios
probably have little reproductive significance.
The minimum duration of continuous copulation of aquarium
drills is listed as follows i
1. 4 h rs. 39 m inutes 5, 2 h rs. 54 m inutes
2 . 4 hr s. 35 »» 9. 2 h rs. 24 "
3. 4 h rs. 35 tt 10. 2 h rs. 17 ”
4. 3 h rs. 34 H 1 1 . 1 hr. 50 ”
5. 3 h rs. 25 ♦I 1 2 . 1 hr. 21 11
6 . 3 h rs. 10 r* 13. 1 hr. 14 "
7. 3 h rs. 14, 53 m inutes
Only one pairing was observed in its entirety (No. 4 in list);
all others were in progress when first seen or observations were
interrupted.
It is quite common for copulating pairs to cease activity, remain
in position, and then resume. One pair copulated for 1 hour, 21
minutes, ceased for 5 hours, 9 minutes and then resumed copulating,
this time for more than 3 hours, 10 minutes. Another pair copulated for three hours and ten minutes, stopped for five hours and fifteen
minutes, and started again. This pair was copulating eleven and a - 32 * half hours later. A third pair copulated for thirty minutes, ceased for four hours and seventeen minutes, and resumed for three hours and twenty*seven minutes.
Copulating females were usually larger than the males with which they paired (Table 5).
Promiscuity may exist in nature because marked captive individuals of both sexes copulated with various partners. A single pair was seen together nine separate times from April 9 to May 25, 1956 in an aquarium.
The female copulated with another male on April 25 and the male with other females on April 12 and April 23, Table 1 illustrates the occurrence of promiscuity for marked caged animals.
Pairings apparently occur at all times of the day. Fifteen were seen in the morning, six in the afternoon, and twelve in the evening in aquaria. Although these differences may indicate diurnal periodicity, equal observational effort was not expended during the day. Seasonal periodicity of copulation was determined by watching for copulation in aquaria. Unfortunately these observations were not made regularly, thus the curves in Figure 9B may not be entirely accurate. However, they are of interest because they are roughly similar to the seasonal periods of copulation in cages. In the fall of 1955, copulation was seen as late as the end of October and early November. It was resumed early in April 1956, and reached a peak in early May. A few pairings were - 33
Table 5. Length-frequencies of copulating drilla.
Total length mm. Pairs in Pairs in Pairs and Trios Midpoint of range aquaria 1936 cages 1956 cages 1957 ______2 ___ s£______2 ___ s£...... 2 .... rf ......
14.5 1 15.5 1 16.5 1 2 1 1 17.5 0 5 5 5 18.5 0 4 10 8 19.5 2 3 2 10 20.5 1 0 6 11 6 21.5 3 3 6 10 1 4 22.5 6 7 7 5 3 1 23.5 2 2 10 20 6 24.5 4 12 5 1 25.5 1 2 5 26.5 3 1 3 27.5 2 2 28.5 2 29.5 1 30.5 1 - 34 -
observed through August 11 end a late wave of copulation occurred in
October. The temperature range at which copulation was seen in aquaria
was from 52*F to 83* F. In 1956, 60 caged drills (30 of each sex) in a
single compartment were examined every two days for copulation and
egg«laying between the hours of two and five in the afternoon (Fig. 9C).
The onset of the spring copulating period was not recorded because the
experiment was not established in time. Pairing was first seen in late
April at a temperature of 56.5*F, reached a peak on June 17 at 74.5*F,
and ended on July 8 at 77* 5*F. A total of 98 pairings was observed. A
small wave of copulation during the week of August 26 may have been
stimulated by a slight drop In temperature. A late wave totaling 24
pairings began at the end of September when the temperature was 71* F and ended on October 28 at a temperature of 64* F. Observations made two or three times a week during the winter of 1956*57 revealed no
copulatory activity. This was expected because the snails appeared dormant and were either partially withdrawn, lying free on the bottom of the cage or clinging loosely to oysters on the bottom itself. Bata recorded in 1957 from two cage compartments containing 45 drills each (5099 and
40 efcf) are given in figure 10C, which shows that copulation in the two groups was much less intense than in the previous year. Fairings were first observed on April 1 when the temperature was 51 *F. There was no distinct peak in the curve and after the week of May 6 activity regressed - 35 -
CD O ~ BJ
♦ ft
-«| - s 2 spawning spawning in 1956.
So
S3SV0 993 30 W30WnN Fig. Fig. 9. Seasonal patterns, grouped weeks, by of temperature, copulation
X33M U3d NV3W SNOIJ-VTOdOO 30 U38»inN SNOIiVindOO 30 H39WDN S3SV0 993 30 838M0N 1I3HN3UHV3 S33893Q - 36 -
o f termination termination of observations. catches, catches, copulation, and spawning in 1957. Vertical bars indicate
/.va U3d dVdi 83d Fig. 10. Seasonal patterns, grouped by weeks, of temperature, boring, trap HOJ.VO d o 3 V i.0 i ATX33M S3SV0 D93 30 «38«r»N
333M U3d HV3M SONIUOB 30 BSBHMnN SNOIlVnOdOO 30 H38W0N S3SV0 0 0 3 JO UBflMON 1I3HN3UHV3 S33M03O steadily downward to July 8 at a temperature of 79* F. Most of the copulatory activity occurred slightly earlier in 1957 then 1956, probably a result of higher temperatures.
Copulation data from buoyed traps are sparse. Xn 1956 just four possibles were seen, two pairs and two trios. Xn 1957, five were observed.
Xn each case, the participants were in the usual position with the female attached to an oyster and the male on her right ventral side. Although these pairs were lifted and separated no penes were seen; however, as mentioned before, it is probable that they had been actually in copula because this position is not normally assumed unless sexual activity is occurring.
Because many animals brought in from nature began almost immediately to copulate in the finger bowls, it is possible that this activity may be stimulated by such a disturbance. Overwintering of ipermatozoa in females
Stauber (1943) observed that a female U. cinerea, isolated from
April to October, laid fertilised eggs at the end of that period* This female may have retained sperm for a year because it was believed to have been inseminated the previous summer. Because we wished to know whether E. caudate possessed the same capability, eight females were taken from cages or natural bottom during late fall and winter of
1956-57 and held individually in cage compartments. Two aquarium-held females known to have copulated in the fall of 1955 were also isolated and observed. A brief history of these females is given in Table 6 in which their egg case production and viability of embryos are included. The evidence indicates that females can retain viable spermatozoa for at least sin months and probably longer. It seems likely that part of the sperm retained over winter are received during the fall copulatory period.
Because two females isolated in 1955 deposited non-viable embryos In 1957
(really not embryos if not fertilised, but complexes of vitelline bodies and ova), it appears that they were unable to retain living spermatozoa through two winters. Three of the females did not oviposit. Two of the three exhibited growth in 1957 and one showed evidence of much recent growth when taken from the bottom. Despite the fact that one female had copulated several times in an aquarium in the fall of 1956, the occurrence of growth probably indicates that these individuals were immature. Table 6 . Reproductive histories of females isolated during 1956-57 with a record of 1957 egg case production and v ia b ility of embryos.
Time in month isolated from History Number Embryos male to of of Deposition Embryos per deposition of female esa cases periodliving Case la st case
--mm; copulated 8 Nov 1955, iso lated 10 Jan 1956 in aquarium; deposited 7 viable 9 1 June- No Not cases 16 May 1956, a ll lo st 6 July counted 18 except one having liv in g veligers; moved to cage on 31 Jul* 1956,
-- mm; copulated 7 Nov 1955; iso lated 10 Jan 1956 in 48 15 June- No Not aquarium; did not ovip osit 20 July counted 18.5 in 1956; moved to cage 31 July 1956.
26,8 mm; caged with male 29 27 May- Yes 9-31 6 4 Aug 1956 to 31 Nov 1956; 6 June isolated 31 Nov 1956.
26.8 mm; caged with male 46 1 June- fe s 13-25 6 4 Aug 1956 to 31 Nov 1956; 22 June isolated 31 Nov 1956, % 23.7 mm; collected from 36 29 June- Yes 6-31 6 bottom between 24 Nov - 6 July Dec 1956 and eased.
2 1 .6 am; co llected from 4 29 June- Cases - 4 bottom 25 Feb 1957 end 6 July lo st cased,...... _..„ .
2 2 .2 mm; co llected from 55 18 May- Yes 7-16 4.5 Wormley*s Rock 13 Mar 1957 6 July and cased. Although the numbers of isolated females, seven, may be too few to be significant, it is possible that females deposit fewer cases 1st the absence of males. The numbers of cases deposited in this experiment per female (mean number of cases 33.4, range 4*55) was about 22 less than those produced during both summers by 31 caged females isolated with single males. . 41 *
Seasonal Activity
Little is known of the seasonal activity of individual animals
of any gastropod species. To study this aspect of their life history, 45
JEi ca**d**a individually marked with airplane dope were caged on March 2 ,
195?. Their cage was lifted at two-day intervals and the activity of each
drill noted. Particular attention was paid to copulation, oviposition and
drilling. A pair In copulatory position was recorded as copulatieit if
the male exhibited the penis or groove when lifted. An individual was
recorded as drilling if over a freshly bored hole. Positive identification
of an ovipositing female is often uncertain; however, a female seen amidst
a cluster of new cases in the normal egg-case depositing attitude was
considered to be the one which deposited them. Seventy-five lifts were
made from April 4 to September 6 .
Figure 1OC shows that copulation, which began two weeks before boring, was the earliest recorded activity of the drills. Later copulatory
activity was interspersed with feeding in both sexes, (Table 7). Only three females were observed ovipositing during this period. Although
unfortunate for our purposes, this reduced oviposition in cages corresponds to the reduced spawning in natural populations in 1957. One female may have copulated after ovipositing (the observation was uncertain). Over half the females were not observed copulating during the period and several individuals were not seen boring. On the average females were found - 42 -
Table 17. Seasonal activity of Individual caged E. caudata. summer 1957. Number identifies individual drill, C - copulation, number after C is individual it copulated with, 0 - oviposition, F - boring, ? means uncertain observation, D means animal dead on date given.
A23-29 A30-S5 Individual Sex M29-A4 A5-11 A12-18 A19-25 A26-M2 M3-9 M1Q-16 M17-23 M24-30 M31-J6 J7-13 J14-20 J21-27 J28-J4 J5-11 112-18 J19-25 J26-A1 A2-8 A9-15 A16-22 *FF *** .FF .F. FF .F F.. * . . *.* • •• .FF F.. F... .F.. D3Aug k ■ 0 2 0 Jul c 2 7 f . FFF F0?F .F. ..F. F.C3 4 . FF.. .F. .F. .F.. ..F FF. FF. ;. f Y . t . ..F. .FF .F. FF D3Aug c27 F.. .014 Jul .F .F . .F. FF.F F.0?C28 FF. .F.. .FF . . F .F F... F.F D3Aug FF F FF. F..» FF. •C33F F.. FF.F FF F C30*>28--F *c33 FF. ..r FF.F ..FF FF.F .F. .F F C2s.. J m FFF ..F .F. FF.. .C3 4 .. F... FFF D3Aug D3Aug .F. .FF. FF. FFF FFF FF.F FF.! ..F .F ..F ..F. .F. F.F ..F .FF. • • ..F .FF. F.. .F. F... FF.. ..F .F FF • •• .F. i f . . !.F .FF 0 2 0 Jul r .F F.. F.F FFF FFF F.. F. F FF F. • . .F . F
maies F.. F. . 027Jul 23 •F F D6Jul 24 .! -cal. 25 ..F. F.F .... ! ! r .F. 26 ..rc u F.. FF.. .F. FF. 27 DllAug C8 •* 12 C4 .; 28 F. . D20Jul C1 2 * * .CU F ,*!!f FFF FF. ..F F.F. F. .C« FF. 29 . . F .F. F.. F.F ..FF .FF. .FF 30 CJ1 ** •••• 31 ..F ...F D3Aug 32 ..F 33 . c i o . F. . D20Jul F 34 .F. .C12C4 . F.. F.. 35 .F...... C11 .F.
o activity by any animal when cage hauled.
es and four males were inactive during every observation and are not • 43 * seven times in drilling position during the 75 lifts* but males only about tbree times. Since drilling and feeding normally persists for several hours or days* it is likely that a good proportion of this activity was seen and thus probable that many of the individual differences noted herein are normal. Continuous copulation* which lasts at most only a few hours* was undoubtedly missed in many individuals.
In 1957* traps with fresh lames River seed oysters were placed in the experimental area in late March and records of their catches were kept the entire summer. Catches were negligible until the week of April 29 when the mean weekly water temperature rose from 60.5* F to 6 6 . 5*F (Fig. I OB). Then the catch increased steadily to the week of
May 13* when the temperature was 6 8 * Fj thereafter* the catch declined at an even rate to July I and only small numbers came onto the traps until August 26. Most traps were then rebaited* and large catches were recorded again. Several traps were left with the original oysters* and the catches remained very low although they did increase slightly. Data collected by Dr. 1. I*. McHugh showed that catches of U, cinerea on traps* baited with oysters not changed during the summer* were smaller in July and August than they were in spring and fall. This pattern seems to support the work of Janowics (1957) who found that drills are attracted to growing oysters, McHugh (personal communication) stated that oyster growth at
Gloucester Point occurs in spurts in the spring and fall. Soon after rebaiting* • 44 -
the numbers diminished q u ic k ly as the smallest seed and the barnacles
and mussels were consumed and the catch of September 23 was about
the same as the low catches of the period from July I through August 19.
The traps were rebaited again on September 26, but this time catches were less than half the size of those of August 26, undoubtedly because of
decreased activity caused by the cooler water temperatures. Again the
catch dropped off quickly and drills were scarce after the week of October 7 as the water temperatures dropped below 64* F. Stauber (1943) and McHugh
(1957) also reported that rebaited traps catch more drills. These catch records and cage observations show that this species is active for only about six or six and one-half months a year. Andrews (1956) found that g. caudate came on traps for only about six months at Wormleyfs Hock in the York Hiver.
Drilling observations in the cage were totaled and compared with weekly trap catches (Fig. 10B). Caged animals commenced boring at a temperature of 54, 5*F, about two weeks before drills came on traps; thereafter boring activity lagged trap catches by a week or more. They parallel each other roughly, however, and both diminished to a low point during the first part of August. Since large catches were obtained the week of August 26, the animals presumably were still active and probably the decreasing catches and reduced frequency of boring in July and early
August mirror the decreasing attractiveness of the bait andnot complete inactivity tr aaativation of tba animals. After rebaiting hi* tvapi about the middle of July, Andrew* in 1954 obtained hi* largest catches of E,
caudate during the lattar ball of July and through most of August at
Wornkiay,a lock. • 46 -
Spawning period nmri iv --"inrTy- 'Wrrn II iiirnn--rn- n
The spawning period was studied by Engle (1935) in Bela ware Bay
and Andrews (1956) in the York liver. Both workers recorded the numbers
of E. caudata and U. cinerea egg cases in their traps, In Delaware Bay
eases were deposited during the period May £3 to July 25, with greatest
numbers during the week of June 13, Perhaps because his sample was
smaller (110 cases), Andrews found the duration of spawning even shorter,
June 13 to July IS. These workers found that the spawning period of IT.
cinerea is of longer duration than EL caudata because it begins earlier
in the spring and extends later into the summer. Although not noted by
these workers, other studies on U. cinerea have reported a second smaller
spawning in some summers with the peak usually securing in September
(Cole, 1942; Oaltsoff al., 1937; Stauber, 1943).
Egg cases for this study were collected from traps and a cage.
During 1956, 12 traps were fished between the laboratory and ferry piers.
All drills were removed each time. Spawning began on traps and in the
cage about May 20 at a recorded temperature of 65° F (Fig, 9C and D).
The peak occurred during the week of June 1? when the mean temperature was 77. 5* F. Thereafter it diminished and ended late in July. In the
cage the peak occurred about one week later and ceased in early August.
A small flurry of oviposition which occurred on August 26 probably was
stimulated by the slight decrease in temperature. - 47 -
In 1957* 15 traps ware eat out in each half of the experimental area. All individuals on the upriver half were scattered about the bottom after being counted and measured so that the population would be disturbed as little as possible. Spawning began in the cage on May IS at6 8 *F and on traps about May 20 at 69* F (Fig. 10C and 0). There was no distinct peak and spawning was much less intense than in 1956. Tr* ,p* were placed in a new section of the experimental area for three and one*half days during the week of June12 , and 78 cases were deposited. This one record for a half*weekly period is twice as high as the record of any other full week and therefore may be abnormal. Hargis (personal communication) reports that E. caudate egg cases in comparable eel* grass areas were negligible in 1987 as compared to 1956. The effects of decreased spawning in 1957 became apparent when no identifiable speci* mens of age*group8 were collected on traps until October 3* In contrast many small drills were collected by late August and September in 1956 when egg cases were more numerous.
Factors causing spawning fluctuations remain unknown, but perhaps spawning is closely dependent upon intensity of copulation, which may be influenced by as yet unknown factors.
It is felt that egg*case deposition may be interrupted or inhibited by the frequent lifting of traps and that the numbers of cases may be too low. As an example, only five clusters (49 cases) were obtained from * 48 -
12 traps down river hall of the experimental area in 1957; whereas, a few hundred cases were collected from that area on shells. Hew cases were also collected on shells after spawning ceased on traps.
These findings agree with Engle’s in Delaware Bay, hut are more extensive than Andrews. There was no late wave of spawning of K. caudate egg c a se s. - 49 -
Intensity and duration of oviproduction
Several studies have been made on intensity and duration ol ovi production in U. cinerea hut the results are probably not very significant because in the absence of a technique for live-sexing* the actual numbers of females under observation were not known (Carriker 1955). Various earlier authors have estimated that U. cinerea females deposit about 45 to 50 eases in a breeding season. He!son (1922), Engle (1940)* and Cole
(1942) have stated that U. cinerea do not deposit all their cases at one time* but may lay several clusters in a breeding season.
Because nothing was known of this phase of reproductive activity for E. caudata* experiments were designed to determine the number of egg cases deposited by individual females of various lengths. Graded pairs of females and males from the smallest to the largest available sises were put into compartments of three cages on May 16 before spawning had begun. In another cage* the compartments housed pairs each about
20 millimeters. Several one-and two* year-old oysters were placed into each compartment and replaced on August 10. The cages were cleaned weekly when egg cases were counted* but the drills were measured every four weeks. The experiment was continued in 195? with the same animals* but the original oysters were not changdd. Missing or dead animals were replaced by May II* 1957. All cages were examined and cleaned periodically during the winter. - 50 -
Intensity
The mean number of egg cases per season for each female was
55.0 cases with a range from 2 to 174 (Table 8 ). Because it was not then
known that Eupleura females do not deposit egg cases in their second
summer, the 1956 experiment was not well designed to show intensity in
that it included many young drills, and only II of the 30 identifiable females were reproductively active. Comparisons of oviproduction for
the two years from these data may not be justified, since differences
between the two years may have been caused by factors, such as kinds
and amounts of food, that were not carefully controlled. Also, it is not known if fertility of males changes with time. These comparisons, how
ever, are tabulated for interest (Table 9).
Females retained from 1956 and reproductively active for the first time in 1957 laid an average of 77.1 cases. Two females did not repeat their 1956 oviposition in 1957.
One-hundred and thirty-six clusters containing about 19 cases each
(9. 8 ) were deposited by 23 caged females in 1957. The mean number of egg cases contained in 232 clusters from shells collected randomly in the experimental area was about nine cases (S. 7). Comparison of the frequency distribution of number of egg cases per cluster in cages and from bottom shows that they are significantly different {^|L2 * 9.70, d.f. » 4, JP less than 0. 05) (Table 10). Various factors may influence the slues of clusters, * 51 •
Table 8 . Duration and in ten sity of spawning by individual caged females.
I n itia l Length Duration Number of Total tear am (weeks)______weeks inactive eg a cases
19.4 8 2 63 20.7 8 1 61 21.1 7 0 95 2 2 .0 1 clu ster 0 2 1956 23.3 8 1 46 23.0 4 1 17 24.1 10 3 45 25.7 5 0 37 or 38 26.7 6 1 25 or 26 27.8 2 0 29 29.0 8 1 95 6.6
19.7 7 2 54 20.0 3 1 15 21.7 11 0 174 23.0 4 1 37* 23.0 5 0 49 23.7 4 0 64 23.8 1 clu ster 0 9 23.7 6 2 71 24.3 10 4 71 24.4 8 3 45 1957 24.7 6 0 68 24.8 8 2 79 25.2 2 0 14 25.3 3 0 22 25.7 9 1 114 25.4 7 2 28 26.0 1 clu ster 0 2 26.0 8 1 76 26.3 7 3 60 27.6 12 4 107 32-3 4 0 37 6.7 S3 (1956 & 1957!
* Loat Jun. 8 and excluded fro. man • 52 ■*
tabla 9* Comparison of Ibc total nuabar of casas dapositad by individual cagad fanaloa In aueoaaalva yaar».
Individual.... 1954 ___ 1952
1 41 54
2 43 45
3 95 15
4 29 60
5 25 or 24 22
6 44 9
- ...... I ...... -. 4 5 . 21 52 39
% fa b le 1 0 • Conparlsen of suobtri of eaiti per clutter on theilt in tin experimental area, with those deposited by eeged f settles* summer 1957.
Re. of eases Cages hauled Cage hauled per each natural ♦ every clu ster week bottom two weeks* d ^ i - s 1- 5 31 31 49
6*10 44 60 26
11*15 49 51 I 6
16-20 6 16 1 2
21*36 6 * 0 J&Z ! 65 _ _ 3 ______l M _____ i e Rot compared in text with other two distributions. such as availability of food, or interruptions, but the actual cause of this
difference in clusters are unknown. Nevertheless, the clusters were approximately the same size. Observations of particular compartments over a period of a few weeks showed that females deposited small clusters of cases, desisted for a short period and resumed this activity later. The average was about six clusters per female (range1 to 13 clusters) during the 1957 spawning season. Then the only unknown is the munber of clusters females in nature deposit.
It appears as though the number of cases deposited by a female is independent of her size because the smallest 14 of 31 females deposited an average of 53.2 cases; whereas, the largest 17 individuals deposited an average of 51. 5. A comparison of the distribution of number of cases shows no evidence that they are different « 0.03, d.f. * 1, P * 0. 8 6 ).
Duration
Duration of the egg-laying period cannot be stated with precision" \ from these data because cages were hauled only once a week and estimates may be as much as two weeks too long, one week at each end of the season.
The average duration for 10 of the 11 females in 1956 was approximately seven weeks ( 6 . 6 ) (Table 8 ). One female which oviposited in only one week was left out of this average because it usually takes less than a day for a female to deposit a cluster. In 1957 the average maximum time of egg-laying of 18 of the 21 identifiable females was also seven weeks(6.7). Two which oviposited only one cluster end one which was lost were not
Included. The spawning period lasted approximately nine weeks In 1956 and eight weeks in 1957 (Figs, 9C and IOC). These cage data thus indicate that a single female may spawn throughout most of the spawning season. m 56 »
Sites of egg-case deposition
In 1937, three targe collections of cases were obtained by hand- picking shells from the experimental area (Table 11). The most common shells in this area were those of dead hard clams Mercenaria mercenarla
(L.}, or live clams partly exposed, and dead and live oysters, Crassostrea virginlca (Gmelin). Jingles, Anemia simplex Orbigny, worm tubes, and often growths of red sponge. Microclona, were living on these shells.
Dead jingles and Tagelus plebius Solander were also found loose on the bottom. Most shells were free of E. caudata egg cases. Cases were always attached to hard surfaces and no preference for jingles, worm tubes, or the foundation shell itself was obvious. The only evident requirements for these substrata are that they be hard and free of fouling.
Occasionally U. cinerea cases occurred in similar sites. Most cases were deposited upright in a vertical or sub*vertical position# but a few were found distal end down. Probably because E. caudata does not climb, no cases were found on eSlgrass blades or pier pilings, where U. cinerea cases occur in numbers.
It is possible that females do not necessarily return to their old spawning sites to oviposit because it was seen that new clusters were deposited in various places about compartments which caged one female.
They may seek out favorable sites regardless of whether cases are already there or not. • 57 *
Table 11. Subatrata of | . caudata egg caaea
Type* of observation* subatyata
Experimental area Empty hard clans 50 Living and dead oysters 25 Live hard clans IS Bead jin g les Bate S&g&M ElSfciS* 10 Stones B ottles
Otter tten «tev» Base o f eelgraaa Bead transverse ark clam Live blood ark elans All rare Rotten wood Live Sj. cinerea
Field cagea Otter tten «b Live ribbed mussel Live and dead bamaelea Live |* caudata Percentage not Plaatle screen determined Masonite boarding Sheet plastic Aquaria Otter tten «bove Metal tack Percentage not Glass wall determined . 58 - Description of cases and embryos Fgg cases of the rough drill are leathery, vase-shaped capsules which may he distinguished from those of other gastropods in this area by two distal projections. The larger of these projections is a hemispherical operculum which covers the aperture through which hatching concha will emerge. The other is a solid extension of egg case material. The case itself is triangular in cross section. A longitudinal seam or suture extends from one side of the stalk distally along one triangular edge of the case over the operculum, dividing it into halves, and down the middle of the broad side to the opposite side of the stalk. Similar sutures in egg cases of the muricids T. laplllus and Oeeaebra erinacea 3U were described by Fretter (1941), and in 0. cinerea by Hancock (1956). Figure 11 illustrates possible variation in shapes of cases and lengths of stalks, and also shows that both distal projections are not always present. The seam does not always occur in the same plane of each case, though it always runs over the middle of the operculum. A few anomalous cases were observed with sections of their wadis missing, but with embryos still in normal position. The color of the case changes with time. When first deposited it is almost translucent except for the opaque cap and does not have the bluish cast described by Pope (1910*11), Carriker (1955), Oanaros (1957) for jl, cinerea cases. In two or three weeks the color changes to deep yellow, and after the conchs have emerged, to dark brown. Cases - 59 - Fig. 11. Variations in the shapes of E. caudata egg cases. Figures _ x 6*3."' - Etching in drawings shows direction of surface granulation, but it is not actually as distinct as shown. A-H. Normally shaped cases. D. Most common shape. I-P. Unusual shapes. I. Mark in suture is natural. K. Stalk with odd wing-like protuberences. N-P. Cases with only one point. • 60 - collected in the experimental area in 1956 averaged 7.7 mm in length (6 . 0 minus the stalk), and 1. 8 m m in width. The range in length was 5. 2 m m to 11. 0 mm. Cases collected at Tillage's oyster ground averaged 9. 2 m m , ( 6 . 9 mm), and 2.4 mm, and ranged in length from 7.4 mm to 1 1 .3 mm. Whenever a female was observed depositing cases, measurements were made of her length, and the length of the cases. Usually larger females deposited larger cases hut there was considerable variation in this attribute (Table 12). Perhaps actual measurements of the soft parts would have shown a closer correlation. Measurements were made of the majority of cases deposited by known caged females in 1956. The data for each half of a female's spawning season were lumped and the totals for each half compared. The data show no indication of a difference (first half mean « 7.27, number » 170, S(x»x)^ * 4245.65$ second half mean » 6.98, number * 154, S(x*x )2 * 2047.77s + t » 0 . 60, P 0. 50). Thus it is possible that the size of a female's cases does not change much during a spawning season. Within freshly laid egg cases the embryos form a loose clump sus* pended in a jelly*like albumen. Early embryos are spheHcal and usually pale yellow, though many are white. A few are yellow, light tan, light orange or purple. Carriker (1955) stated that U. cinerea embryos are yellow to orange in color. Necrotic encased embryos usually turn purple. * 61 * Table 12. Relationship between shell length of S. caudata females and the •m b length of eases they deposited^ a tamers of 1956 and 1957. (Caged and natural populations). length of Length of R ubers Ijeeale in...we. m * t„ M.m 2 0 .1 6.52 59 20«5 6.42 41 2 1 .1 7.10 48 2 1 .1 7.80 6 2 2 .2 7.54 14 23.4 7.96 25 23.5 7.70 2 24.0 7*12 6 24.1 8.17 3 24.3 9.01 14 24.8 7.19 26 25.4 8 .1 8 25 26.0 9.93 10 26.5 9.05 8 26.8 7.86 18 26.9 8*11 14 27.5 8.19 19 28.0 7.49 6 • 62 - Live, apparently normal, protoconcha with purple vitelline bodies were occasionally seen. When locomotory organa developed, embryo a moved freely within the case until they hatched, but often late proto concha became so crowded that movement was impeded. Forty-two freshly-laid embryos averaged 9.36 mm (range 0. 34- 0 .3 9 m m ) in diameter, the same sise reported by Carriker (1955) for 0. cinerea embryos. Fifty-four hatching concha, measured as they assumed purchase about foe apart are of foe case, averaged 0 .9 m m (range 0 . ? - 1 .1 mm) in greatest length. E. caudata has non-pelagic larvae. After emergence foe young concha crawl down thesides of their cases and about the substrate to which the case was attached. Occasionally a tubular non-colled individual, looking otherwise normal, appeared. Although somewhat similar, JB. caudata protoconchs differ from those of 0 . cinerea in that the siphonal canal of late stage protoconchs is less heavily-tinged with purple; foe two protoconchs can be distinguished by this character. - 63 - Numbers of embryos per case In 1935 Haskin showed that E. caudata in Cedar Creek, oil Barnegat Bay, New Jersey, deposited more embryos per case than 0. cinerea. In his studies, 445 cases from traps and cages averaged 22. 2 embryos each (range 8 to 42), and 1,29? U. cinerea cases averaged 8 .1 embryos each (range 0 to 20). According to Carriker (1955), six similar studies of U. cinerea report averages varying from 8 . 0 to 11.0 embryos per case (Brooks, 1879-80; Pope, 1910-11; Nelson, 1922; Federighi, 1931; Stauber, 1943; Adams, 1947). In this study, nine samples of cases (Table 13) were collected during the years of 1956 and 1957 to determine (1) whether the same numbers of embryos per case would be obtained at any time during one spawning season; (2) whether there were variations from one year to the next in a particular area; (3) whether there were local differences in drill populations around Gloucester Point; and (4) whether cases deposited by caged Eupleura contained different numbers of embryos than cases laid on natural bottom . To determine whether numbers of embryos per case varied through out the spawning season, three large samples were collected from the experimental area in May, June, and July 1957, covering the spawning season. The results give evidence of heterogeneity (F « 4. 3, P>0. 01 <0. 05). There is no evidence that the June and July samples are different (t= + 0.42, Table 13. Numbers of embryos per case In various samples collected at Gloucester Point and T illa g e 's oyster ground (summers 1956 and 1957). No. of Iwbryo. P«r c«». ... Location Source Date cases mean ranee Parlance Experimental handpicked May 28- 277 12*6 1-24 17.01 area sh ells 30, 1957 M it Jun 15* 349 13.5 2-27 16.24 17, 1957 Jul 1- 166 13.3 1-27 18.36 22, 1957 buoyed May 28- 210 15.8 5-35 27.70 traps Jun 28, 1956 Jun 1- 187 14.5 6-32 27.40 Jul 19, 1957 Cage experimental cage May 24- 262 15.2 3-32 23.57 area Jun 30, 1958 Cage 5 very large, ” Jun 9- 184 2 1 .2 10-37 23.33 aixed; local and Jul 4, Wormley Rock d r ills 1956 Tillage’s oyster dredged May 13- 157 18.4 6-36 30.86 ground oysters Jul 2, 1956 it M Jun 13, 283 2 0 .2 3-34 20.13 Cage Tillage’s cage Jul 3- 90 19.5 8-47 49.35 ground 24, 1957 • 65 - P a 0£ 0 ); therefore, the difference lies in the May sample. Not enough information was collected during this study to support an explanation of these results. Statistical comparison of the data comparing the numbers of embryos in cases collected on traps in the experimental area for 1956 and 1957, shows an Indication of an annual difference, (* * * 2.15, P « 0.04). The data for the two years from Tillage's oyster ground appear to be different, also (t » + 4. 46, P<0.001), These data do not show a consistent trend, however, as cases in the experimental area had slightly fewer embryos in 1957, but those from Tillage's ground had slightly more. The samples were collected in slightly different parts of Tillage's ground in 1957, which may explain the difference. Because the samples (1956 and 1957) taken at Tillage's ground are different from the samples collected in the experimental area, this is good evidence that local populations differ in this feature. Statistical comparison did not show that caged females deposit different numbers of embryos per case from those which oviposited on traps (F = 1.27, P (90 eases but included only a few clusters) to be analysed, but the mean, 19.5 embryos per case is close to that of the sample collected from the bottom in 1956, 18,4 embryos per case, A small selected collection of » 66' - very large females held in cage 5 deposited an average of 21.2 embryoe per caee. These data indicate that the characteristics o£ the female more closely determine the numbers of embryos per case than environmental fa cto rs. A record was kept of the variation in numbers of embryos each known caged female deposited in most of her cases. The data show that there was considerable variation (Table 14). This contrasts with the findings of Cole (1942) who stated that there was little variation in numbers of U. cinerea embryos per case deposited by a single female. 67 - Table 14. Variation in numbers of embryos per case deposited by individual caged females* summer 1956. Preveliger Stage Onshelled Veliger Stage Frotoconch Stage Ho. Ho. Ho. Female Cases Mean Variance Cases Mean Variance Cases Mean Varianee h 18 1 2 .1 4.85 33 11.4 5.81 8 12.4 4,55 B 15 10.5 9,27 29 1 0 .1 3.63 7 7.8 5.29 C 24 8 .2 2.78 28 7.9 3,29 28 8,7 2,69 D 12 21.9 11.43 8 2 0 .8 4.27 9 19.3 19.38 % 14 19,9 1.64 30 19.4 4.17 15 8,7 6 ,1 2 P 1 26 * s 19.8 14,55 10 2 2 .6 7,32 6 5 14.2 3.70 11 14.6 11.27 7 14.5 3.27 H 6 19.0 25.60 9 m 1 12 s» X 7 14.1 1.14 10 16.0 30.65 11 18.8 30.36 J 8 9,3 6.84 1 10 • 17 1 0 .8 1.72 Table IS. Variation in numbers of embryos per case deposited by female E in Table 14. Ho. of Preveliger* Onshelled* Protoconch* emhrvos ... -...__ ...stage...... veligerstage ..-...... stagf 4 • e 1 5 ♦ « 1 6 • e 1 7 • 2 2 8 * 1 2 9 2 8 3 10 3 7 1 11 5 5 3 12 2 4 * 13 2 I 1 14 • 1 • 15 s e e 16 s e e 17 e I e ♦Frequency distributions not selected to shoe reduction in progressive stages of development. - 68 - Incubation period Knowledge of the incubation period of E. caudata embryos may have important practical implications in control measures because it might be used to determine the best time to destroy egg cases. Several workers have collected data on this subject for JUN cinerea in other areaf and their results vary widely. The most careful work has been done by Ha skin (1935)* Cole (1942), and Ganaros (1956). Haskin (1935), working in Delaware Bay, held egg cases in field cages at temperatures ranging from 74*/f , and reported incubation periods lasting from 18 to 25 days. Cole (1942), in England, found incubation periods to last from 27 to 32 days when cases were held in the laboratory at temperatures averaging 72. 7* F. At Milford, Connecticut, Ganaros (1956) determined the incuba tion periods of embryos held in the laboratory at constant temperatures. The first concha held at 70. 5* F were released in 30 days; those held at 77*F, in 22 days. Egg cases of E^ caudata were collected from traps and one cage every two days, left on their original substratum, and placed in clear perforated plastic cups suspended from the laboratory pier in a tray one foot from the bottom. Two or three clusters containing several egg cases each were used for most determinations. Cases were examined every two days for hatching embryos. Termination of the incubation period was defined as the time when over one-half of the cases in a particular cluster had released at least one conch. Although slightly uneven development was observed in the present study, no attempt was made to record incubation . 69 - periods of individual embryos. An experiment was designed to determine whether holding cases in perforated cups influenced the incubation period. For this purpose, oysters bearing egg cases were attached to a rectangular wooden board by elastic bands. Because the board collected algae, tunicates, and silt, it closely resembled the bottom. Cases were held both in cups and on the board for comparison. Table 16 shows that there was very close agreement in hatching times of embryos in different clusters of the same age, and that holding cases in perforated cups did not influence the incubation period. The incubation periods lasted from 24-31 days at a mean temperature of 70* and shortened as the temperature increased, _e.jg. , at 79. 8 *F it lasted only 14-16 days. Probably as a result of higher temperatures in 1957 than 1956, incubation periods were shorter. Comparing the results of E. caudata with those obtained for JJ. cinerea at similar temperatures the incubation period is two to seven days shorter. To be reliable*however, comparisons should be made from data collected in the same area and under similar experimental conditions. Table 16* The incubation period of Ej. caudate embryos, Temperature during period(°F) Bate Number Batching Incubation laid of eases .....d ate...... period (days) mean rang# Cup May 18*23 4» June 15*17 24*31 70*0 65.0-76.5 M May 28-30 m June 19*21 21-25 74*2 66.5-76.5 May 28*30 m June 19*21 21-25 May 28*30 m June 19-21 21-25 June 11*13 12 June 29*July 1 17*21 76,5 71.5*80.5 June 11*13 10 June 29-July1 17*21 June 11-13 21 June 29-July 1 17*21 June 18*21 13 July 5*7 15-20 77*8 71.5*81.5 June 18*21 8 July 5*7 15-20 June 18-21 3 July 5-7 15*20 II June 27*29 4 July 13-15 15*19 78.8 77,0-81*5 tt June 27*29 7 July 13*15 15-19 tl July 5*7 4 July 20*24 14*20 78*0 77.5-78.5 July 5*7 6 July 20*24 14*20 July 14-16 11 July 29-31 14*18 78*2 77*0-79.0 July 14*16 5 July 29-Aug 1 14-19 July 14-16 -*» July 29-Aug 1 14-19 July 24-26 5 or 6 Aug 10*12 16-20 77,8 76,0-79.5 July 24-26 5 or 6 Aug 10*12 16-20 1957 Cup May 14-16 14 June 6 -8 21-25 71*0 67,0-73.5 Board May 14*16 10 June 6 -8 21-25 Cup June 15*17 5 June 28-July1 12-17 79*2 76.5-81.0 Board June 15-17 6 June 28-July1 12*17 Cup June 24*26 9 July 8 -1 0 13-17 78,9 77.5-80.0 Board June 24*26 6 July 8*10 13*17 Board June 24*26 16 July 8*10 13-17 Cup July 4*6 13 July 19*21 13-17 79.6 78,5-80.5 Board July 4*6 12 July 19-21 13-17 Board July 14-16 6 July 30 14-16 79.8 78,5-81,5 - 71 - Percentage of embryos reaching protoconch stage B. caudate females do not include nurse eggs (nourishing embryos) within their egg cases as do some related gastropods, £,j|. T. lapillus^ (Korschelt and Heider, 1890 ). Fortman (1926 ) and others believe that nurse eggs are produced by fertilization of normal ova by atypical sperma* tozoa. Evidently such embryos fail to develop normally and serve as nourishment for the normal embryos. Microscopic examination of gonad smears of caudata males shows only one type of spermatozoon. Over 3,000 egg cases, containing embryos in various stages of development, yielded no nourishing embryos. Usually ail embryos in each case were about equally developed. Undeveloped embryos were seen so rarely that it seems likely that they were caused by normal aberrations which appear in any population of dioecious animals. To establish the numbers of embryos which successfully attain the prehatching or protoconch stage, embryos in 37 freshly*deposited cases were counted. These egg cases were then isolated in separate compartments of a plastic box held in an oyster tray suspended in the river. Ninety*three per cent (range 81. 8*100) of the embryos in these different cases developed fully. The numbers of embryos at each embryonic stage were similar In 361 egg cases deposited in cages (preveligers 12.49, 110 cases; unshelled veligers 12.04, 143 cases; protoconchs 12.81, 108 cases. . 72 . Predators and associates of egg cages Large numbers ol egg cases were found to be devoid of embryos even though the operculum was still in place. Closer observations revealed holes in the sides of most of the cases. The most common hole was a C-shaped slit about 0. 8 m m in width and; therefore, large enough to serve as a possible ex it for emerging concha, At least one case with a slit still contained a few undeveloped embryos; some clusters contained slit cases but also unperforated cases with live embryos, therefore, it seems unlikely that these openings are exits for concha, but rather made by pre* dators bent on feeding on the contents. Less frequently evidence of predation was manifested as round or oval holes of varied sizes but always too small to permit the exit of concha. Occasional egg cases bore jagged tears and at times most of the case was torn away. In the laboratory mud crabs