YEAR-ROUND PRODUCTION OF RIPE GAMETES
BY BENTHIC POLYCHAETES IN
BISCAYNE BAY, FLORIDA!
J. KNEELAND McNULTy2 AND NELIA N. L6PEZ
Institute of Marine and Atmospheric Sciences,
University of Miami
ABSTRACT
Four of the most abundant benthic polychaetes of Biscayne Bay, Florida,
contained ripe gametes throughout one year of observations. They are
Lumbrineris impatiens, Leanira grubei, Owenia fusiformis, and Chaetopterus variopedatus. The absence of recurring seasonal cycles of abundance
of the benthic polychaetes, shown in earlier quantitative work, is interpreted
to be the result of steady year-round recruitment of young.
INTRODUCTION
The ecological importance of benthic polychaetes in Biscayne Bay,
Florida, is evident from past studies, yet the biology of local species remains
largely unknown (McNulty, 1961, 1966; McNulty et ai., 1962; O'Gower
& Wacasey, 1967). This gap in knowledge makes it difficult to evaluate the
stability of the level-bottom communities of animals or to reach conclusions
ultimately on their productivity and significance in the Bay's food chains.
Accordingly, the authors studied gametic maturity of six of the most abundant species of benthic polychaetes over a 12-month period to ascertain
their spawning characteristics and to reexamine their role in local benthic
animal communities.
Specimens were obtained as part of a benthic research program instituted
by Dr. Hilary B. Moore. Large numbers of locally abundant benthic
species including polychaetes were procured for autecological studies. Field
samples were taken in two areas-in area B of previous work and in area
C, which is adjacent to, and an extension of, area A of previous work
(McNulty et ai., 1962). Area B (lat. 25°40.5'N, long. 80 09.9'W), in
the Cape Florida Channel, 0.9-1.5 km northwest of the old tower at Cape
Florida, has a depth of 3 to 4 m and a bottom of sandy mud. Area C
(lat. 25°44.1'N, long. 80 11.0'W) is 0.7-1.5 km south of the Intracoastal
Waterway drawbridge span in the Rickenbacker Causeway, has a depth
of 3 to 4 m and a bottom of soft mud. Data from the two areas have been
combined in the analyses which follow. Samples were taken from November
1965, through October 1966, at approximately monthly intervals. Both
0
0
1 Contribution No. 1102 from the Institute of Marine and Atmospheric Sciences, University of
Miami. This study was supported by Grant No. WP 00573 from the Department of Health, Education and Welfare.
• Present address: Bureau of Commercial Fisheries Biological Laboratory, St. Petersburg Beach,
Florida.
946
Bulletin of Marine Science
[19(4)
authors participated in field sampling and analyses. The sampling device
was a conical bucket dredge. Sediment samples were washed through three
successively finer screens down to I-mm aperture.
The species in descending order of abundance were: Lumbrineris
impatiens (Claparede), Leanira grubei (Treadwell), Owenia fusiform is
delle Chiaje, Chaetopterus variopedatus (Renier), Pista cristata (0. F.
Milller), and Terebellides stroemi Sars.
Dr. Jervis W. Wacasey and the senior author identified the polychaetes
initially, and Dr. Marian H. Pettibone of the Smithsonian Institution,
Washington, D. C., confirmed our identifications. Reference specimens are
housed at the Smithsonian, except for Chaetopterus variopedatus; its
identity did not seem to require confirmation. The assistance of Drs.
Wacasey and Pettibone and the constant guidance and encouragement of
Dr. Moore are acknowledged with sincere thanks.
All specimens of whole polychaetes from this study are preserved in
chronologically numbered bottles, and permanent slides of diagnostic parts
of many specimens are on file. A project notebook contains the numbers
of the bottles, sketches of the slides to show the arrangement of dissected
para podia and mouthparts, and all other project data. The specimens and
notebook are in the possession of the senior author.
METHODS
Gametes from live animals were examined as soon as possible after
field trips. The integument of each live animal was pricked with a needle
to obtain coelomic fluid with its contained gametes. Observations were
recorded according to the following arbitrary scale of ripeness of gametes:
1. Ripe: with motile sperm, or with eggs whose nuclei were not visible.
2. Intermediate I: with mostly motile sperm, or with mostly eggs whose
nuclei were not visible.
3. Intermediate II: with some motile sperm, or with some eggs whose
nuclei were not visible.
4. Intermediate III: without motile sperm, but with developing sperm;
or without eggs whose nuclei were not visible, but with developing eggs.
5. Negative: without sperm or eggs.
The nucleus of some fully developed eggs was faintly visible, so the
phrase "whose nuclei were not visible" is relative. As eggs approached
maturity, their nuclei became increasingly indistinct. The size of eggs
also gave a useful indication of relative ripeness, but too few data were
collected for conclusive results. Sperm cells exhibiting vigorous activity
within a few minutes of removal were considered to be fully ripe, while
those showing no activity were obviously unripe. Judgement on intermediate conditions of both eggs and sperm was subjective but meaningful,
because experience clearly showed discernible degrees between extremes.
1969]
McNulty & Lopez: Production of Gametes by Polychaetes
947
LUMBRINERIS IMPATIENS
LEANIRA
GRUBE!
OWENIA FUSIFORMIS
CHAETOPTERUS VARIOPEDATUS
1001
50
o
.-:
:> !oJ
(,)
(,) 0
PER CENT
o
WITH SOME
Z
0
RIPE GAMETES
1. Percentage of individuals of four species of benthic polychaetes
with some ripe gametes. Dashed line means either no sample was taken that
month (Jan.), or fewer than three individuals of a species were taken (Chaetopterus in March, and Owenia in Aug. and Sept.).
FIGURE
The ripness of eggs and sperm believed to be ripe was confirmed in most
cases by conducting artificial fertilization experiments.
RESULTS
Ripe gametes were found throughout the year in all four of the most
abundant species: Lumbrineris impatiens, Leanira grubei, Owenia fusiformis, and Chaetopterus variopedatus. Stated with reference to the
arbitrary scale of ripeness described under Methods, some individuals of
all four species were placed consistently in the Ripe, the Intermediate I,
or the Intermediate II categories each time samples were taken (see Table
1). Figure 1 shows the percentage of individuals with at least some ripe
gametes throughout the year. The figure was constructed by expressing
the total number of individuals in the three higher categories of ripeness
as a percentage of the total number of individuals of a species taken in each
sample. L. impatiens alone of the four species showed a seasonal decrease
in production of ripe gametes in October, November, and December. The
reproductive pattern of the two less abundant species, Pista cristata and
Terebellides stroemi, is not clear, because relatively few individuals were
taken each month. Ripe gametes were found on most occasions, but the
results are inconclusive (see Table 1).
948
at Marine
Bulletin
[19(4)
Science
TABLE 1
GAMETIC CONDITIONOF SIX SPECIES OF BENTHIC POLYCHAETES
(Expressed as numbers of individuals)
Intermediates
Fully
ripe
Date
(;
I
(;
Q
Q
Lumbrineris
Feb.
Mar.
Mar.
May
June
June
July
Aug.
Sept.
Oct.
(;
Q
(;
gametes
Q
2
2
2
2
3
1
2
4
1
3
1
3
2
1
4
1
1
1
2
1
c&Q
Total
impatiens
1965
13 Nov.
9 Dec.
1966
1
2
30
4
2
29
6
2
7
20
No
III
II
1
3
1
3
1
1
2
2
2
2
2
3
4
3
2
2
4
4
1
5
1
2
4
3
5
4
3
4
3
15
11
17
8
6
20
1
9
24
4
6
7
7
17
25
20
12
3
7
14
29
18
26
24
&
1
3
4
3
1
1
2
Total:
231
Leanira grubei
1965
13 Nov.
9 Dec.
2
1
1
3
2
1
1
2
1
6
4
4
2
3
6
2
9
2
16
8
9
7
3
6
34
26
18
23
11
1966
1
2
30
4
2
29
6
2
7
20
Feb.
Mar.
Mar.
May
June
June
July
Aug.
Sept.
Oct.
2
8
1
1
1
1
4
1
2
4
6
3
4
3
1
2
1
5
2
3
1
1
&
Total:
7
6
1
5
2
5
3
1
1
3
1
2
2
6
5
2
9
2
8
1
4
11
4
2
23
16
29
25
229
1969]
McNulty & Lopez: Production of Gametes by Polychaetes
949
TABLE 1 (Continued)
Intermediates
Fully
ripe
Date
5
II
I
Q
5
Q
5
III
Q
5
No
gametes
Total
Q 5&Q
Owenia fusiform is
1965
13 Nov.
9 Dec.
1966
1
2
30
4
2
29
6
2
7
20
Feb.
Mar.
Mar.
May
June
June &
July
Aug.
Sept.
Oct.
1
1
2
4
3
5
1
1
1
2
3
3
3
5
3
10
3
2
1
2
2
2
2
3
2
2
5
1
3
1
1
1
3
2
1
Total:
Chaetopterus
Feb.
Mar.
Mar.
May
June
June &
July
Aug.
Sept.
Oct.
Total:
3
2
0
11
96
1965
13 Nov.
9 Dec.
1966
1
2
30
4
2
29
6
2
7
20
3
7
8
14
11
22
15
2
1
1
2
1
1
4
1
1
variopedatus
2
2
1
1
1
11
5
2
2
3
1
9
6
12
4
1
1
1
1
4
3
3
2
3
1
2
1
1
1
1
3
2
1
1
2
2
1
1
6
2
1
1
1
2
1
2
1
1
1
1
5
19
10
4
5
85
950
of
Bulletin
TABLE
~
1 ( Continued)
Intermediates
Fully
ripe
Date
[19(4)
Marine Science
I
2
~
2
8
No
gametes
m
II
2
8
2
8&2
Total
Pista cristata
1965
13 Nov.
9 Dec.
1966
1 Feb.
2 Mar.
30 Mar.
4 May
2 June
29 June &
6 July
2 Aug.
7 Sept.
20 Oct.
1
1
1
2
1
1
1
1
1
1
1
3
1
1
3
3
1
3
7
2
1
5
2
4
3
13
1
0
6
2
1
1
3
1
3
2
3
1
1
Total:
45
Terebellides stroemi
1965
13 Nov.
9 Dec.
1
1
1
2
1
1966
1
2
30
4
2
29
6
2
7
20
Feb.
Mar.
Mar.
May
June
June &
July
Aug.
Sept.
Oct.
1
1
2
1
2
1
1
2
1
2
2
1
6
7
1
4
0
1
1
1
1
1
Total:
Grand Total
1
2
1
1
1
26
712
1969]
McNulty & Lopez: Production of Gametes by Polychaetes
TABLE
951
2
DRY TISSUE WEIGHTS AND NUMBERS OF POLYCHAETES FROM
AREAS A AND B COMBINED
All polychaetes
Dry tissue weight
Date
No. of individuals
(No./m2)
(g/m2)
1957
August
1958
January
April
August
October
1959
January
April
July
Mean:
0.7873
29.0
0.6519*
0.4397
0.8373
0.5151
39.8
27.6
77.2
17.9
0.5669
0.4355
0.5407
20.1
28.8
21.3
0.5968
32.7
• Owenia not included. There were 1,926 individuals per square meter, weighing 1.7451 grams per
square meter, in the samples from area B. This great abundance occurred only once in two years of
sampling.
TABLE
3
DRY TISSUE WEIGHTS AND NUMBER OF INDIVIDUALS
OF ALL INFAUNA FROM AREAS A AND B COMBINED
All infauna
Dry tissue weight
Date
(g/m2)
1957
August
1958
January
April
August
October
1959
January
April
July
Mean:
• Owenia excluded. See footnote, Table 2.
No. of individuals
(No./m2)
4.6923
180.0
4.5904*
2.5842
4.2446
2.6302
182.3
249.9
277.5
118.2
3.3122
3.7028
4.3653
109.6
256.8
151.1
3.7653
190.7
[19( 4)
Bulletin of Marine Science
952
6.0
ALL
5.0
INFAUNA
4.0
3.0
N
E
...•.•
~2.0
I-
::x::
(!)
lLl
~
lLl \.0
::::l
(/)
~O.8
I-
~ 0.6
0
0.4
AUG.
1957
FIGURE
2.
JAN.
APR.
1958
AUG. OCT.
JAN.
APR.
JUL.
1959
Dry tissue weight of all polychaetes and all infauna, from quantitative study of 1957-59.
The individuals of the four most abundant species made up over 70
per cent of the total number of polychaetes sampled each month, and
Lumbrineris and Leanira were consistently foremost in abundance. Contrary to expectations, Owenia remained generally abundant. The findings
in 1957-59 were that its appearance was sporadic, short-lived, and concentrated (Tables 2 and 3). There were many samples taken by the bucket
dredge in recent work in which Owenia was poorly represented or absent,
and others in which it was plentiful. Thus, the local distribution of Owenia
is patchy, and the earlier samplings either sampled the patches or missed
them entirely.
In the light of subsequent studies, it is pertinent to reexamine the data
on polychaetes from 1957-59. Two major purposes of the earlier work
(McNulty, 1961; McNulty et at., 1962) were to describe typical macro-
1969]
McNulty
& Lopez:
Production
of Gametes by Polychaetes
300
o
200
N
E
..••..
ci
z
~
(/)
-l
ALL
INFAUNA
ALL
POLYCHAETES
953
100
80
60
<{
::::)
0
>
0
40
Z
LL
0
0::
W
co
:E
::::)
20
Z
10
AUG.
JAN.
1957
FIGURE 3.
Number
of individuals
APR.
AUG. OCT.
JAN.
JUL.
1959
1958
of all polychaetes
APR.
and all infauna
per square
meter, from quantitative study of 1957-59.
invertebrate bottom communities of south Florida and to study their structural stability and possible seasonal fluctuations over a 2-year period. A
lho-m2 Van Veen grab and sieves with mesh openings of up to 1 mm were
used. At approximately quarterly intervals, 1.6 m2 of bottom was sampled
at both areas A and B. The polychaetes totalled 15.8 per cent of the dry
tissue weight of all infauna and 17.1 per cent of the number of individuals
of all infauna. Neither on the basis of dry tissue weight nor numbers of
individuals did the polychaetes as a group exhibit a recurring seasonal
cycle of abundance (Tables 2, 3; Figs. 2, 3). Reexamined in the light of
present knowledge, regularly recurring seasonal changes in abundance are
[19(4)
Bulletin of Marine Science
954
unlikely, and the observed fluctuations are regarded as random variations
in sampling.
Perhaps the most significant aspect of this study is the documentation
of year-round breeding. This is less common in the tropics than some
workers have believed. Of 12 species studied on the Great Barrier Reef
by Stephenson (1934), only three bred throughout the year, and only
one of these, a hydroid, bred uniformly. Dr. H. B. Moore (personal communication) states that, of tropical invertebrates living at least one year,
a current study indicates that about 25 per cent breed throughout the year.
All four of the polychaetes studied here bred throughout the year, and
three of them apparently uniformly. Year-round breeding is more probable
in short-lived species. Some polychaetes are believed to live for more than
one year in temperate waters. Growth rates tend to be high, and longevity
low in tropical seas (R. B. Moore, personal communication), so it is
possible that the high proportion of continuous breeding is to be associated
with short lifespan.
SUMARIO
PRODUCCI6N
ANUAL
DE GAMETOS
BENTICOS
EN
MADUROS
BISCAYNE
BAY,
POR
LOS POLIQUETOS
FLORIDA
Cuatro de los mas abundantes poliquetos benticos de Biscayne Bay,
Florida, presentaron gametos maduros durante todo un ano de observaciones. Ellos son: Lumbrineris impatiens, Leanira grubei, Owenia fusiformis y Chaetopterus variopedatus. La ausencia de ciclos estacionales
recurrentes en la abundancia de los poliquetos benticos, demostrada en
trabajos cuantitativos previos, se interpret a como resultado del constante
reemplazamiento de los j6venes durante todo el ano.
LITERATURE CITED
McNULTY,
J. K.
1961. Ecological effects of sewage pollution in Biscayne Bay, Florida:
sediments and the distribution of benthic and fouling macro-organisms.
Bull. Mar. Sci. Gulf & Carib., 11(3): 394-447.
1966. Recovery of Biscayne Bay from pollution. Doctoral dissertation, University of Miami, Coral Gables, Fla., 178 pp.
J. K., R. C. WORK, AND H. B. MOORE
1962. Level sea bottom communities in Biscayne Bay and neighboring areas.
Bull. Mar. Sci. Gulf & Carib., 12(2): 204-233.
O'GOWER,
A. K. AND J. W. WACASEY
1967. Animal communities associated with Thalassia, Diplanthera, and
McNULTY,
sand beds in Biscayne Bay. I. Analysis of communities in relation to
water movements. Bull. Mar. Sci., 17(1): 175-210.
A.
1934. The breeding of reef animals. Part II. Invertebrates other than corals.
Scient. Rept. Gt Barrier Reef Exped., 3(9): 247-272.
STEPHENSON,