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STUDIES ON SPECIATION
IN MALDANID
POLYCHAETES
OF THE NORTH AMERICAN
ATLANTIC
COAST.
II. DISTRIRUTION
AND COMPETITIVE
INTERACTION
OF FIVE SYMPATRIC SPECIES1
Charlotte Preston Mangum
Department
of Biology,
Yale University,
and Duke University
Marine
Laboratory
ABSTRACT
The geographic and ecological distributions
of five species of maldanid polychaetes have
been characterized.
Maximum density of each species occurs in areas where the species
does not live sympatrically
with other maldanids, even though these areas may not occupy
the central portion of its geographic range. A more intensive investigation
in Beaufort Harbor, North Carolina, indicates that the sympatry of all five species is accompanied
by the
reduction of total maldanid density.
In the sympatric situation, three spccics are differentiated
ecologically
with respect to
depth, sediment composition,
and substratum utilization.
The remaining two spccics, C.Jymeneh torquata and C. xonalk, are completely sympatric yet undiversified
in their utilization of the substratum for tube-building
and feeding.
The possible importance
of an algal
pigment, accullmlatcd
by C. torquutu but not by C. xonulis, is discussed.
INTHODUCTION
The annual reproductive
cycles of C.
torqunta and C. mucosu were investigated
by Wilson ( 1882), Bookhout and Horn
( 1949)) Moment ( 1951)) Newell ( 1951))
and Mohammad
and Bookhout
( 1959).
The occurrence and hab,itat of shallowwater maldanids have been reported in ecological surveys (Allee 1922; Cowles 1930;
Stauffcr 1937; Clark 1942; Pearse, Humm,
and Wharton 1942; Burbanck, Pierce, and
Whitely
1956; Carpenter
1956; Sanders
1956, 1958, 1960). But the factors governing their distribution
and density have
been largely ignored.
In a survey of the bottom fauna of
Mcncmsha Bight, Massachusetts, Lee (1944)
comments at length on one of the more
conspicuous maldanids, C. torquata.
Its
maximum density per unit volume of scdiment was the largest of all species encountered, although the variation over the total
study area was considerable. He concludes
that its abundance is associated with depth
and with the nature of the bottom, although
its scarcity at some stations is unexplained.
Sanders et al. (1962) report that great
densities of C. torquntn, an important component of their Barnstable Harbor, Massachusetts, intertidal community, are found in
stable well-sorted sediments of fine sand.
The soft-bottom fauna of Atlantic coastal
waters frequently includes members of the
polychaete family Maldanidae. As is often
true of numerically important polychaetes,
our knowledge of their biology is quite
fragmentary.
The present contribution
is
part of a larger study of intra- and interspecific divergence in the five species
Clymenellu torquatn ( Leidy ), C. xonalis
( Verrill) , C. rnucos~ ( Andrews ), Bmnchio,asychis americuna Hartman, and Petaloproctus socialis Andrews. Classification of
the three species of Clymenelln Verrill was
revised earlier (Mangum 1962a).
All of these worms are tubicolous and
infaunal. From sand and mucus they construct vertical tubes which are inhabited
head downwards.
The tail shaft usually
appears a few mm above the substratum
surface, and the head shaft terminates approximately
8-30 cm below the surface.
Feeding is accomplished by the ingestion
of sand grains and detritus from the depth
of the head shaft, followed by egestion into
the water.
-~-___
1 Part of this investigation
was supported
by
National
Science Foundation
Grant G-17862.
It
was prescntcd for the degree of Doctor of Philosophy in Yale University.
12
ECOLOGY
OF MALDANID
A more intensive ecological investigation of
the same species (Kenny, unpublished data)
suggests that the range of sediments supporting
dense populations
is cxtrcmcly
small. The ecology of other maldanid spctics is virtually unknown.
I am indebted to Dr. L. M. Passano for
his sponsorship, and to Dr. W. D. Hartman,
Professor I. E. Gray, and Professor G. E.
Hutchinson for their criticisms of the manuscript. Dr. II. L. Sanders has been an
invaluable critic and welcome companion
on several collecting trips. Facilities were
kindly provided by the following institutions : Atlantic Biological Station, St. Andrews, New Brunswick; Mount Desert Island Biological Laboratory, Salsbury Cove,
Maine; Muscum of Natural I-Iistory, Natucket, Massachusetts; Department of Rcsearch and Education, Snow Hill, Maryland;
Bears Bluffs Laboratory, Wadmalaw Island,
South Carolina; Marincland Research Laboratories, Marincland, Florida; Institute of
Marinc Biology, University of Puerto Rico,
La Parguera, Puerto Rico.
METIIODS
Population
density
The geographic area examined covers the
coast of continental North America from
New Brunswick to northern Florida, and
one locality in the West Indies. Quantitative estimates of population density were
obtained during summer months at several
localities (Table 1). Except at Beaufort
Harbor, North Carolina, the depth of maximum density was initially determined, and
subsequent sampling was confined to that
depth. Specimens were collected by passing spadefuls of sediment through a Z-mm
mesh sieve. Density values were obtained
by taking ten pairs of nonoverlapping
0.1
m2 X 0.2 m samples, and multiplying
the
mean of each pair by factor 10. The result
is expressed in number/m2 of substratum
surface. Two or three entire square meter
areas were excavated to prevent bias due
to patchiness or aggregation.
In Beaufort Harbor, North Carolina,
where the five species occur sympatrically,
estimates of species density changes with
13
POLYCIIAETES
depth and sediment composition were desired. The upper limit of a transect 10 m
wide was marked off at 5 dm above mean
low water, and paired 0.1 m2 X 0.2 m
samples were taken at each l-m interval
to a depth below which no maldanids occurred. The resulting transect dimensions
were 10 X 10-20 m, or 100400 m2 in surfact area. The transects were moved along
the shore at approximately 50-m intervals,
and the sampling repeated three times.
Scdimcnt samples were taken from the
depth of maximum density at five gcographic locations (Table 1) by removing
a cylinder of 30&500 g ( dry wt ) from the
substratum surface to 20 cm below it. They
were rinsed several times with distilled
water and dried overnight at 105C. All
samples were taken in duplicate and each
subsamplc pretreated in one of two ways:
1) dispersal with N-NaOH and redrying,
or 2) gentle grinding with a rubber-tipped
pestle. The sediment material was allowed
to pass for 20 min through a graded series
of U. S. Standard sieves, driven by a motor
shaker. Each fraction was weighed and the
result calculated as per cent total weight
of all fractions.
Niche specificity
In view of the interesting sympatric situation in Beaufort Harbor, North Carolina, it
seemed important to define the niches of
these five species populations more prcciscly. The particle-size composition of substratum utilized in tube-building
and feeding has been measured and compared.
Worm tubes at Station 1 at Pivers Island
and Station 2 at Bird Shoal were collected
over a period of several weeks in the summer until the total weight of each sample
amounted to 50-150 g ( dry wt ) . The tube
samples were pretreated and sieved exactly
as the parent sediment samples, described
above. Discrepancies between the observed
particle-size composition of the tube material and the sediment from which it is
derived were tested by chi-square.
It was necessary to devise another method
of analyzing the size distribution of particles
ingested by the worms, since the amount re-
14
CHARLOTTE
PRFSTON
quired to give reliahlc results by sieving is
much larger than that contained in thousands of worms. The guts of 25 individuals
of four species were emptied onto microscope slides and the contents mounted in
Permount. The first 100 particles from the
left on each slide were measured with an
ocular micrometer, giving a total of 2,500
particles per species. Unfortunately,
Brunchioasychis americana is so rare at this
latitude that as many as 25 individuals have
not been collected. No data on the gut
contents of this species are available.
The measurements were grouped into the
same six size classes used for tubes and
parent sediments, and the number in each
class calculated as a percentage of the total.
The results are frequencies rather than
weights, so direct comparisons with parent
material cannot be made.
Sixe of individuals and
predation pressure
Age structure was estimated by determining the frequency of size classes within
a population, and by noting their sexual
condition.
Samples of 100 individuals
of
each species present at seven geographic
localities (Table 1) were preserved in 5&%
formalin in seawater. The sample from an
eighth locality, Nantucket Harbor, Massachusetts, contained only 21 individuals.
After larval development, Clymenella torqunta and C. rn~~osa possess a definite segment number (Wilson 1882; Bookhout and
Horn 1949). Growth occurs only by the
enlargement of segments already present.
Since a large number of the individuals in
a population are regenerating lost segments
at any one time, the values for these species
were corrcctcd for missing segments. As
each segment occupies a constant proportion of the animal’s total length, missing
segments were noted and corrections made.
The other three species possess indefinite
segment numbers, and growth occurs by
the continuous addition of new segments as
well as enlargement of old ones. Only nonregenerating individuals
of these species
were measured; the percentage of the populations undergoing regeneration was de-
MANGUM
termined separately. The results may be
influenced by the changing incidence of
predation with age and size.
The replacement of lost tail segments is
believed to indicate injury to the worm by
a predator. Injury by mechanical disturbance is not likely to bc responsible for high
regeneration frequencies in protected cnvironments.
This hypothesis is supported
by the extremely low frequency of anterior
regeneration in natural populations.
Only
the tail emerges from the tube during the
normal activity pattern of the worm. Thercfore, predation pressure has been estimated
from the percentage of a sample undergoing
posterior regeneration.
Hydrography
Hydrographic
data have been obtained
from sources cited below. Where no citations are given, the mcasuremcnts were
made by the author. Salinity was determined with a glass hydrometer.
ZOOGI~OGBAPHY
AND
Passamaquoddy
HABITAT
Bay
The northernmost station is a scmiprotected shore of Passamaquoddy Bay near
St. Andrews, New Brunswick (45” N lat,
67” W long), The substratum consists of
coarse gravel to medium sand interrupted
every few meters by sizable boulders. The
sandy portion is only lo-20 cm deep owing
to an underlying layer of rock. This scemingly harsh environment is more densely
populated by C. -torquata than any other
Atlantic Coast station. Since C. torquata
tubes usually attain 20 cm in length, the
lower head shafts of these tubes are curved
and frequently cemented to the hard rock
surface. Fig. 1 shows mean monthly temperature values from nearby surface waters
in 196&61, kindly supplied by the staff
of the Atlantic Biological Station. Despite
the relatively low temperatures throughout
the year, the minimum is no lower than
winter temperatures recorded frequently by
the author in Long Island Sound. Waters
in this area arc generally free from ice, even
during the coldest months.
ECOLOGY
OP M ALDANID
BARNSTABLE
HARBOR
20
15
POLYCHAETES
(40’30’ N lat, 70’15’ W long). Sparse C.
torquntn populations are found in medium
to fine sand in the Ice of a rock jetty protecting the harbor entrance.
10
z
e
Long Island Sound
0
I
= 90
s
p:
w
10
2
E
0
LONG ISLAND
SOUND
Bradley Point is located at West Haven,
Connecticut, on the shore of Long Island
Sound (39’30’ N lat, 73” W long). Dense
C. torqunta populations inhabit fine sand
off a semiprotected tidal spit formed at the
point of land. Temperature values at the
water-substratum
interface are given in
Fig, 1; salinity fluctuates between 18.3 and
29.3%0.
;f.+$z+~:ARG”ERA
JFMAMJJASOND
1. Seasonal variation
at six localities.
FIG.
of water tcmpcrature
Western Bay
Western Bay of Maine (44’30’ N lat,
68’15’ W long) is a narrow body of water
separating Mount Desert Island from the
mainland. C. xoruzlis is found in coarse to
medium sand occupying a sheltered cove,
Western Bay (2) in Table 2. C. tolrqunta
inhabits a much finer sediment several miles
away, on a protected flat in the Ice of the
causeway from the island to the mainland,
Western Bay ( 1) in Table 2. The midday
temperature at the substratum surface in
September 1961 was 2OC, several degrees
higher than in the nearby Bay of Fundy.
The salinity of Wcstcrn Bay was 31.45, at
the time of collection.
Barnstable Harbor
Barnstable Harbor is an inlet off Cape
Cod Bay, Massachusetts (41’30’ N lat,
7O”lS W long), whose hydrography
and
ecology have been described by Sanders
et al. ( 1962). Very dense C. torquata populations inhabit sediments of medium to
fine sand. Dr. A. C. Redfield has kindly
provided
temperature
data from West
Barnstable Landing ( Fig. 1). The values
for Barnstable Harbor waters are generally
higher than those for surrounding waters.
Nantucket Harbor
Nantucket Harbor is a semiprotected inlet off Nantucket
Sound, Massachusetts
Isle of Wight Bay
The Isle of Wight Bay is formed by
waters from the Chincoteague and Assawoman bays as they empty into the Atlantic near Ocean City, Maryland (38”2U N
lat, 75”20’ W long). Moderate densities of
C. torqunta occur in medium to fine sand
in this protected bay. A 6-year average
( 1951-56) of temperature indicates that
surface waters fluctuate between 5.5 and
26C, and salinity between 28 and 32%0. The
data were furnished by the Department of
Rcscarch and Education, State of Maryland.
Beaufort Uarbor
The mouth of the Newport River, North
Carolina (34’40’ N lat, 76’30’ W long),
converges with Bogue and Back sounds as
the three bodies empty into the Atlantic
Ocean. The area of confluence forms the
harbor of Beaufort, North Carolina. The
shores of the mainland are protected by
North Carolina’s Outer Banks, resulting in
a high-salinity,
sheltered environment
of
extensive shoals and sand flats. Within
the harbor, the western shore of Pivers Island supports populations of C. torquata,
C. xonalk, C. mucoisq and Bmnchioasychis
americana. Muddy sand predominates along
most of the length of the island (Stations 1
and 2 in Table 2), giving way to medium
sand at its southwest tip (Station 3 in
Table 2), a point of converging currents.
The temperature data in Fig. 1 were compiled by Dr. G. C. Hughes and Mr. R. P.
16
CHARLOTTE
TABLE 1.
Species
present
Locality
PRESTON
Summary
~
IMaximum
density
( no./mz)
MANGUM
of quantitative
__
70
regenerating
_- ~----~
Mean
length
(CrnkSD)
Passamaquoddy Bay,
New Brunswick
Station 1
C. torquata
675
56
4.6 iz 0.9
immature
Western Bay, Maine
Station 1
C. torquata
250
46
Station 2
C. xonalis
275
48
3.5 f 0.9
immature
5.2 I? 0.6
immature
C. torquata
615”
Barnstable Harbor,
Massachusetts
Station C1
3.6 + 9.3
results
-~_
-
.-~
hlodal
size
class of
sediment
particlcs
(Pd)
spm&ing
.z
Spawning
tcmpcrature
(“C)
62-124
>2,000
125-249”
both
Nantucket Harbor,
Massachusetts
Station 1
C. torquata
50
26
11.4 -1- 2.7
mature
125-249
Late April to
mid-May
12-141
Long Island Sound,
Connecticut
Station 1
C. torquata
275
23
5.2 k 1.1
mature
125-249
Mid- to late
May
12-14
C. torquata
180
48
125-249
Late March to ca. 14
early April
C. xonalis
25
54
C. mucosa
15
47
4.1 t 0.9
mature
4.0 -t 0.3
immature
5.4 & 1.5
mature
Isle of Wight Bay,
Maryland
Station 1
Beaufort Harbor,
North Carolina
W. Pivcrs Island
Station 1
B.
C.
C.
C.
B.
C.
C.
Station 2
Station 3
Rird Shoal
Station 1
americana
torquata
xonalis
mucosa
americana
torquata
mucosa
C. mucosa
P. socialis
P. socialis
Station 2
Summer River, Florida
Station 1
Bahia Parguera,
Puerto Rico
Station 1
* Sanders
et al.
f Mead
( 1897).
C. torquata
C. torquata
C. mucosa
B. americana
C. mucosa
(1962).
?
120
17
15
?
30
18
5:
203
125-249
250-499
12
4.4 2 0.4
immature
250-499
125-249
250
8
3.8 f 0.7
immature
50
2.7 2 0.7
immature
ECOLOGY
OF MALDANID
Kenny. The normal salinity range is 3038g0, which may be greatly extended by
the influx of river waters after a heavy
rainfall.
Nearby Bird Shoal, a coarse to
fine sandy flat which is exposed at low
tide for over 6 km2, supports C. torquata,
C. xor&.s, C. mucosc1, and PetaZop~octus
so&Es. The salinity regime is more stable
because of the isolation of Bird Shoal from
river waters.
Summer River
The Summer River is a small estuary
whose lower end parallels the coast for
several miles before emptying into the
Atlantic Ocean near Marineland,
Florida
(29”50’ N lat, 81” W long). Sparse populations of C. torquata and C. mucosa are
sympatric in medium sand at a bend near
the Marineland
Research Laboratories.
Both species also occur with dense populations of B. americana in muddy sand near
Crescent Beach ( Station 1 in Table 1).
These areas arc shcltercd from wave action.
Temperature data from Atlantic seawater
entering the Marine Studios seawater systcm are given in Fig. 1.
Bahia Parguera
Bahia Parguera is a small bay off the
Caribbean Sea on the southern coast of
Puerto Rico near Parguera (18” N lat, 67”
W long). A series of coral reefs protects
this bay from wave action, and provides an
extensive shallow-water substratum of coral
sand. Dense C. mucosa populations inhabit
sediment near the roots of mangrove trees
on Marguerita Reef. The tempcraturc varies
only between 25 and 28C throughout the
year (Pyle 1962; Fig. 1); the equally
stable salinity rarely falls below 30s0 (U. S.
Department of Agriculture Weather Bureau
1938).
POPULATION
Clymenella
DENSITY
torquata
CZymeneZZa torquata is the most cosmopolitan of the five species. It inhabits sandy
and muddy bottoms from the Gulf of St.
Lawrence (Treadwell 1948) to the Atlantic
Coast of northern Florida, and it appears
POLYCHAETES
17
to be a recent immigrant in British waters
(Newell 1949). It has also been found on
the Louisiana coast of the Gulf of Mexico
( Hartman 1951) .
Its habitat is generally predictable bctwecn Massnchusctts and North Carolina,
where it colonizes protected bottoms of
fine sand. However, the highest density
measured occurs in relatively coarse sediment of Passamaquoddy Bay, New Brunswick (Table 1). Maine and Florida populations are confined to extremely soft sediments containing large fractions of mud and
silt. The restriction of C. torquata to a
narrow range of sediments in the central
zone is indicated by density change at
Beaufort Harbor stations (Table 1 ), and
at stations studied by Kenny (unpublished
data) and Sanders et al. (1962). High
densities in the Beaufort region are found
in sediments with modal size class 125-249
p, although lower numbers occur in a wide
range of sediments.
In the northern portion of its range, C.
torquuta occurs sympatrically with C. xonc~lti or singly, but in the south it is often
sympatric with more than one other maldanid species (Table 1) . The greatest number of sympatric maldanids is found 150
miles south of the Cape Hatteras thermal
boundary in Beaufort IIarbor, North Carolina, where geographic ranges of the five
species overlap. On the western short of
Pivers Island, C. torquata coexists in the
same square meter of bottom with C. xona.Zis,C. mucosa, and Branchioasychis americana. The highest densities of C. torquata
occur not in the middle latitudes of its geographic range, but in high-salinity
waters
and in single-species populations near the
northern limit of the species (Table 1).
Single-species populations of the order of
400-500/m2 do exist in the vicinity of Beaufort Harbor (Kenny, unpublished
data),
but they are found upstream in reduced
salinities. The zone of salinity tolerance by
C. tolrqunta is wider than the zones of the
other species, but these upstream populations are living near their lethal limits
( Mangum 1963).
C. torquata is typically subtidal in waters
18
CIIARLOTTE
6 ,
4
C.. ZONALIS
PRESTON
C. TORQUATA
MANGUM
C. MUCOSA
P. SOCIALIS
,
2 ,
mlw
5
e-
2
I
c
L
w
n
4
6
8
10
12
14
16
--1
18
20
1
DENSITY /M2
FIG. 2. Variation
of population
density with depth in relation
fort Harbor, North Carolina.
The length of the line in the lower
viduals per square meter of substratum surface.
of small tidal amplitude.
Maximum densities at rivers Island stations are attained
2-16 dm below mean low water (Fig. 2).
Populations extend into the intertidal zone
north of Cape Cod where the daily tidal
amplitude exceeds 2 m.
The geographic trend in length of individuals is somewhat confusing (Table 1;
Fig. 3), but their age at the time of collection undoubtedly differs. The samples from
the two northernmost localities, probably
collected shortly after spawning, contain
only sexually immature worms. The mean
length of mature worms, however, obeys
Bcrgmann’s rule. The annual spawning
period lasts only a few days (Mead 1897;
Newell 1951), and the temperature
at
which it occurs is remarkably uniform over
the geographic area for which it is known
(Table 1). Water temperature during the
months following spawning, i.e., the temperature of development and exponential
growth, does vary considerably with latitude (Fig. 1). Ray ( 1960) presents experimental evidence supporting the hypothesis that agreement with Bergmann’s rule
to the mean low water mark in Beauright corner equals one hundrccl indi-
in poikilotherms may result from the development and growth of northern individuals at a lower tcmpcrature than southern
individuals.
Clymenclla
zonalis
Populations of C. xonnlis were sampled
in Mainc and North Carolina (Table 1).
The species is also known from numerous
localities in the vicinity of Woods Hole,
Massachusetts ( Lewis 1897; Alice 1922))
and north of Cape Cod as far as the Bay
of Fundy. Hartman ( 1951) described a
fragmentary individual of similar morphology from the Gulf of Mexico as ?Macroc@
naene elongnta
( Webster), but no further
reports have appeared.
Populations inhabit medium to fine sand
just below mean low water. Variation of
density with depth is virtually
identical
with that in C. torqzcatn (Fig. 2), although
C. xonnlis is consistently outnumbered in
the sympatric situation. The highest density
occurs in the single species population of
Western Bay ( Table 1).
The range of inhabited sediments par-
ECOLOGY
OF MALDANID
19
POLYCIIAETES
.PASSAMAQUODDY
BARNSTABLE
'WESTERN
NANTUCKET
BAY
HARBOR
HARBOR
w
lJ-
259
LONG ISLAND
SOUND
LENGTH (MM )
FIG.
3,. Length-frequency
polygons of samples from six populations
of Clymenelh
torquntn. Passamaquoddy Bay, Western Bay, and Long Island Sound samples taken in Scptcmbcr; Barnstablc Harbor
sample in August; Nantuckct Harbor sample in July; Bcaufort Harbor sample in May.
tially differentiates C. xonnlis, for this spctics is not found in muddy bottoms. It is
sympatric with C. torqunta in medium sand
at Quahog Pond in West Falmouth, Massachusetts, and in extremely heterogeneous
sediment at Pivers Hand in Beaufort Harbor. But it is not sympatric with C. torquuta when the latter lives in more homogeneous muddy bottom at Western Bay.
Here, C. xonnlis colonizes a coarser sediment from which C. torquata is absent
(Table 1). At Beaufort Harbor, C. xonalis
is also sympatric with C. mucosa and Branchioasychis americana, but not with Petaloproctus socialis.
The mean lengths of individuals suggest
a trend of size reduction on a north-south
gradient, according to Bergmann’s rule
(Table 1). The trend is not entirely consistcnt, since the largest individuals known
originate from Vineyard Sound, Massachusetts ( Lewis 1897), and not from the Bay
of Fundy. The reproductive cycle and age
distribution
within a population are com-
plctcly unknown. North Carolina populations have spawned by late May, and new
gametes appear in the coelom by midsummer.
The tubes are somewhat more fragile
and considerably longer (LIP to 30 cm total
length) than those of C. torquata. They
curve at the head shaft and ascend toward
the substratum surface, becoming J-shaped.
The head shaft aperture lies 8-15 cm below
the substratum surface.
Clymenella mucosa
This species is warm temperate to tropical; its northern limit seems to be North
Carolina, where it exists in moderate densities among other maldanids (Table 1).
No single-species populations are known
from this region. Very low densities occur
in the Summer River, Florida, but Carpenter (1956) reports that C. mucosa is quite
abundant on the Gulf Coast. These populations arc not sympatric with Bmnchioasythis americana, which seems to be the dom-
20
CHARLOTTE
PRESTON
inant Gulf Coast maldanid.
The sparse
Summer River populations are sympatric
with both B. americana and C. torquata
(Table 1). C. mucosa attains its greatest
numbers as single-species populations in the
Caribbean, Although quantitative sampling
was not completed, it was estimated that
population density in the coral sands of
Bahia Parguera, Puerto Rico, is 300-400/m2.
C. mucosa is more intertidal than C. torquata, C. xonaZis, and B. americanu at
rivers Island stations in Beaufort Harbor
( Fig. 2). But its high densities are deeper
than those of Petaloproctus sociaZk on Bird
Shoal. Ecological differentiation
is also apparent on the horizontal gradient of sediment change, for C. mucosa is more abundant in the coarser sediments of Pivers
Island (Table 1). However, it does not
colonize the even coarser sediments of Bird
Shoal which support dcnsc stands of P.
socialis. It does overlap with the fringes
of P. socinlis populations on Bird Shoal, so
that C. mucosa is the only species which
coexists in Beaufort Harbor with each of
the other Four.
Insufficicn t numbers were collected in
Florida to provide meaningful values, but
the trend of reduction in individual
size
with latitude is suggested by the results
from North Carolina and Puerto Rico samples ( Table 1) . The age structure of the
Caribbean population
cannot be ascertained, since the breeding season is unknown. It is not likely that a 100% diffcrence can bc attributed to age unless the
breeding seasons arc nearly converse.
C. mucosa constructs a tube oE sand and
mucus, the tail shaft appearing a few mm
above the substratum surface and the head
shaft opening at 15-20 cm below the surface. Females add an additional arm during the breeding season, so that the shape
resembles an upright Y. The animal inhabits one arm, and the other provides an
outlet for its gelatinous egg mass (Bookhout and Horn 1949). The mucus appears
to withstand desiccation, an obvious advantage in the intertidal zone. It does not
harden so much as that of the other species,
with the result that the tubes cannot be
MANGUM
removed from the substratum intact.
The mode of fertilization
in this species
presents an interesting problem. The eggs
seem to pass directly from nephridia into
mucus, which is then threaded out into
the water through one of the tube arms.
Fertilization may be 1) internal, 2) within
the tube but external to the animal, or 3)
within the egg mass, external to the animal
and its tube. Two worms inhabiting the
same tube have been observed on numerous
occasions in the laboratory, but in several
instances the two were of the same sex.
The larvae emerge from egg masses at
11’&14’~ days, and immediately settle to
build tubes ( Bookhout and Horn 1949).
Like C. torquata, there is no pelagic period
in the life history of the animal.
Petaloproctus socialis
From the large numbers found on Bird
Shoal, it is clear that P. socia.Zi.sis an important component of benthic communities
in the Bcaufort Harbor region (Table 1 ),
but it is known only from the type locality,
Bird Shoal ( Andrews 1891). Dense beds
or “forests” of the tubes occur in perhaps
several square kilometers of fairly coarse
sediment (Tables 1 and 2), exposed to
moderate wave action at high tide. They
arc completely separated from C. torquata,
C. xonalis, and B. americana by secliment
preferences, and somewhat differentiated
from C. mucosa by the combination
of
depth and sediment parameters.
As reflected by the specific name, individuals arc extremely gregarious, their rigid
tubes intertwining
so that a discrete clump
may be formed of as many as 10 animals.
Tubes are straight and vertical to a depth
of 10 cm, and then become convoluted in
three dimensions. The straight portion is
the tail shaft; the head shaft usually opens
Constructed of
within
the convolutions.
shell fragments as well as sand and mucus,
the tubes are extremely compact and rigid.
These properties are clearly important to
a soft-bodied animal living in bottom exposed to wave action. The tubes are also
notable for their water retention, which
may be an adaptation to prolonged lowtide exposure in coarse sediments.
ECOLOGY
TABLE 2.
A. Relative
Source
Pivers
Island
(1)
Pivcrs
Ishnd
(2)
weight
OF MALDANID
Results from chemically
of fractions
c.
mucosa xonalis
tttbes
tubes
(3)
Particle
size ( p )
0.25 0.24 0.23 0
2,000
l,OOO-1,999 0.14 0.20 0.84 0
500- 999 0.72 1.47 5.84 0.56
250- 499 5.66 27.84 56.25 5.41
125- 249 63.67 62.44 35.69 73.48
62- 124 16.03 7.43 1.07 19.23
0.30 0.03 0.84
37- 61 8.83
0- 36 4.66 0.04 0.01 0.46
99.96 99.96 99.97
Total
99.96
B. Chi-square
in parent
c.
Pivers
Islnncl
0.10
1.15
3f.29
14.29
47.71
32.98
0.41
0.03
21
POLYCHAETES
pretreated
sediments
B. americana
tubes
samples
and worm
z{$
(2)
tubes
so~~~/is Western
tubes
Bay (1)
0
1.98 20.12 0.62
3.09 19.14 0.09
0.07 0
9.56 24.54 0.18
0.07 0
1.47 1.98 49.99 18.71 6.58
56.12 72.94 34.36 17.30 24.83
33.21 24.44 0.95 0.12 25.45
3.57 0.59 0.02 0.03 21.73
5.46 0.02 0
0.01 20.48
0
99.97 99.97
99.97 99.95 99.97
99.96
Western
Bay
Clymenellu torquata
Clymenella xonalis
Clymenella mucosa
Branchioasychis
americana
Petaloproctus socialis
Pivers Island ( 1) sediment
Bird Shoal (2.) sediment
Clymenella
torquata
-*
X-I
X
X
X
X
X
Cl~menella
mucosa
Branchionsychis
americana
X
X
X
X
X
River
25.77
14.72
15.00
7.12
24.72
11.83
0.66
0.13
0.03,
0.92
11.44
53.02.
18.55
5.79
10.12
99.95
99.95
test of 1) intcrspccific
diffcrcnces
bctwccn tube fractions, and 2) diffcrcnccs
tube and parent sediment fractions at Beaufort Harbor, North Carolina
Species
Summer
(2)
0.08
bctwecn
Pet;&rrctus
S
X
+- = p > 0.05.
Tx = p < 0.001.
There is no information on reproduction,
The Bird Shoal population does not cow
tain gametes from May through September.
Branchioasychis
americana
Bmnchioasychis americana appears to be
primarily subtropical.
No specimens have
been found north of Cape Hatteras, and
only small numbers are found in the warm
temperate waters immediately
south of
Cape Hatteras. The species becomes the
dominant maldanid on the Florida Gulf
Coast ( Carpenter l%S), and is also found
in great numbers on the Florida Atlantic
Coast ( Table 1) .
It is so rare in North Carolina that the
author collected only nine individuals
in
as many months of rather intensive sampling. Since the techniques employed here
would exaggerate the importance of a rare
species, no quantification
of its density in
Beaufort Harbor was attempted. All nine
spccimcns were obtained from pockets of
mud at Pivers Island ( Station 1 in Table 1) ,
10-15 dm below mean low water. B. americcr;na:coexists with C. torquuta, C. xonalis,
and C. mucosa, but has not been found with
P. socialis on Bird Shoal.
Although the modal size class of sediments inhabited by Beaufort Harbor and
Summer River populations
is the same,
there are significant differences in the overall composition (p < 0.01). It is believed
that the mud pockets which surround Beaufort Harbor worms are very similar to the
more homogeneous Summer River substratum, although the similarity is not apparent
from overall composition.
The nine individuals collected in North
Carolina were not sacrificed for length
measurements, but they all exceeded 10
cm in the living state. Preserved Florida
worms are considerably smaller (Table 1 ),
in accordance with Bergmann’s rule.
The walls of B. a.mericana tubes are
thicker but less rigid than those of the
22
CHARLOTTE
TABLE 3.
A. Frequency
of scdimcnt
fractions
PRESTON
MANGUM
Results from
gut contents
from worm guts at Beaufort
IIarbor,
North
Carolina
(per cent &
SE)
__--___
Species
C. lorquata
Particle size ( j4)
2,000
l,OOO-1,999
500- 999
250- 499
125- 248
G2- 124
3761
o36
0
0
0
4.3
48.9
27.0
8.4
11.2
Total
k
iz
+-I-t-
C. mucosa
0
0
0
0.1
28.3
47.4
10.8
13.2
0.9
2.8
1.7
1.0
1.9
99.8
B. Chi-square
+
-L
zk
k
-I
C. zonalis
0
0
0
3.0
41.7
31.9
8.2
15.0
0.0
1.6
1.8
0.8
1.4
99.8
test of interspecific
diEferenccs
Clymenella
torquata.
Clymenetla torquata
Clymenella
xonalis
Clymenella
mucosa
Pstabproctus
socialis
_____-~--
-*
X-t
X
XL 0.9
k 3.1
Zk 2.1
-c 1.2
zk 3.0
99.8
____.
~--_
Species
P. socialis
-
f
k
zk
Ik
2
*
0.2
1.8
1.8
0.3
0.0
0.0
99.8
between gut particles
-__
__~
Clymenella
mucosa
Cl;oyayt;~la
___-
0
0
1.0
48.4
48.3
1.7
0.3
0.1
X
X
X
* - = p > 0.05.
t x = p < 0.001.
other species. The shape is straight and
vertical, similar to C. torquntn, with the
head shaft opening 25-30 cm below the
substratum surface.
COMPOSITION
INGESTED
OF TUBES
AND
PARTICLES
There were no significant differences in
the results from mechanically and chemically pretreated sediment samples, with the
exception of Bird Shoal samples which contained large amounts of shell. The results
from chemically pretreated samples are presented in Table 2.
Tubes of the three species C. mucosu, B.
americnnn, and P. socinlis differ significantly from one another and from their
parent sediments (Table 2B). But the tubes
of C. torquntn and C. xondis do not differ
significantly in their particle size composition from one another or from their parent
scdimcnt. Only three of the five species
selectively utilize the substratum in tubebuilding.
With respect to gut particles
(Table 3)) the differences between C. mucosn, P. socin~is, and the other two are
significant, but not so between C. torquntcl
and C. xonalis. In all cases, either p > 0.05
or p < 0.001.
C. mucosn utilizes smaller particles both
in tube-building
and feeding. The tubes
of P. socidis clearly contain disproportionately large amounts of coarse material,
which consists primarily of lamellibranch
and small gastropod shell fragments. P.
socialis ingests larger particles than the
other species, but the two largest size
classes present on Bird Shoal are virtually
a limitation
absent. This is undoubtedly
imposed by the size of the oral aperture,
which is no more than 1 mm in diameter.
I?. americunn prefers the smaller particles
in tube-building;
this species is usually
associated with clumps of mud.
PREDATION
PRESSURE
Regeneration frequencies do not suggest
that either C. torquntn or C. xonntis, the
nonselective species, is more often attacked
by predators (Table 1) . Summer samples
of all three species of CZymeneZZn gave
values of 47-55% of the populations undergoing posterior regeneration. The incidence
of regeneration, at least in C. torquatn, is
ECOLOGY
OF MALDRNID
not a seasonal phenomenon. Comparable
samples taken throughout
the year yield
values within this range. Predation on P.
soczY& seems to be much lower; a summer
sample contains only 12% replacing lost
tail segments. None of the nine individuals
of B. n~n&cnnn collected in Beaufort Harbor was undergoing posterior regeneration.
DISCUSSION
The most successful species is clearly C.
torquata, which is likely to be the. most
abundant maldanid in boreal to temperate
shallow-water soft bottoms. C. xoru&s, also
a boreal to temperate spccics, does not
reach large densities in the sympatric situation, where it occurs in a fairly consistent
ratio of 1 : 7 to C. torquutn. Among the
stations sampled, it is found at its highest
density as a single-species population in
sediment too coarse for C. tozquata and in
a geographic area north of C. mucosn: and
B. americana ranges. C. mucosa seems to
be most abundant in fine to medium sands
of warmer waters. Single-species populations are rare or absent in the northern
part of its range. Large densities are found
in tropical waters south of the limits of the
other species. B. americaru~ is extremely
successful in subtropical
waters, but its
geographic range is relatively narrow. It
seems to prefer muddier sediments than
the others, for it is absent in homogeneous
fine sand. The rather mysterious P. socinMs
is also cxtrcmely successful at the one
locality from which it is known. It is not
suggested that this species is truly limited
to a single shoal in North Carolina, for
the failure to encounter it elsewhere may
be due to a lower frequency of suitable
habitats. It prefers intertidal areas of mcdium sand, and seems incapable of colonizing the finer sediments dominated by the
other species. Its density does not change
as gradually as that of the other species,
probably because of its gregarious habit.
Single, scattered individuals
do not occur
on Bird Shoal.
From the viewpoint of interspecific interaction, the most interesting locality is
Beaufort Harbor, North Carolina, where
POLYCHAETES
23
overlap in geographic ranges results in sympatry of five species. It is significant that
the total density of all maldanid species at
Pivers Island is considerably lower than
expected from the maximum density elsewhere of each as a single-species population, It is perhaps even more significant
that the total density of all maldanids is
much lower than the density of a singlespecies population of C. torquata only a
few milts upstream.
Niche divcrgencc of three of the five
species is apparent from their ecological
distribution:
1) C. mucosu and P. socinlis
are more intertidal than the other three,
and 2) C. mucosa, B. americana, and P.
so&&
arc all diffcrcntiated
by their scdiment preferences. Diversification
of these
species is also suggested by differences in
their utilization of the substratum, but the
existing overlap implies competition
for
fractions required in common. Partial diversification in each of the examined dimensions of the niche may suffice to permit
outliers of each species to coexist with
others.
All three species are selective in the fractions utilized in tube-building,
and two
are known to contain significantly different
sized particles in their guts, which probably
reflects selectivity.
The use of the word
“selective” is not intended to connote that
the worm chooses particles by trial and
error. Members of the Maldanidae do not
possess the intricate feeding mechanisms
found in polychaete families such as the
Terebellidae
and Chaetoptcridae
( MacGinitic 1945). It seems more likely that
maldanids
are simply able to discern
patches of sediment which suit their particular requirements. The heterogeneity of
Pivcrs Island scdimcnt is conspicuous. Discrete mud balls, l-6 cm in diameter, arc
frequently surrounded by less compact fine
sand. No sediment is completely homogeneous, and the degree of heterogeneity
that exists here may be a prerequisite to
sympatric existence.
C. to-rquuta and C. xonalis are completely
sympatric in Beaufort IIarbor, and at sevcral other localities not considered in de-
24
CHARLOTTE
PRESTON
tail ( Mangum 1962b). The zones of maximum density on both sedimentary (horizontal) and depth (vertical)
scales coincide. Separation occurs only in the northern
portions of their geographic ranges. Mechanisms of divergence, if they exist, must
take some form other than ecological distribution.
But these two species appear to
bc making identical demands on the environment in terms of their substratum
utilization.
An explanation of their sympatry may
lie in the phenomenon of dichromatism.
Discrete populations of C. torquata occur
in one of two color phases : orange or
green. There is no continuous intergradation of one color phase with the other, although age differences in the intensity of
coloration do exist within a population.
Nor is there a clear-cut geographic trend
in the distribution of color phases, although
the frequency of green populations is somewhat higher in warmer waters (Mangum
1962b). C. mucoscz also undergoes the color
change, though the alternatives are red or
green. C. xonalis, on the other hand, is
always orange. The pigment responsible
for green coloration is the bile pigment
mesobilivcrdin,
a chromophore of the photoreactive pigments in blue-green and red
algae ( Mangum 1962b). The basic body
color of the worm is often obscured by the
accumulation of mesobiliverdin
in epiderma1 granules. Color changes in the laboratory have been produced by feeding orange
worms on sediments naturally supporting
green worms, and vice versa ( Rankin 1946;
Mangum 1962c).
The color of the dichromatic species may
reflect the nature of sedimentary microflora, In the absence of suitable blue-green
algae, C. torquatu derives its coloration
from photooxidizable
yellow-orange
pigments, probably
carotenoids.
Green C.
torquata populations also possess the orange
pigments, but they are obscured by the
accumulated mesobiliverdin.
The density
of blue-green algae in these sediments is
thought to be very high. Williams ( 1962)
has shown that blue-green algae, in sediments very similar to those which support
MANGUM
green worms, are second in microfloral density only to diatoms. The present author
h as observed large numbers of a living
blue-green alga encrusting the outer surface of the echiuroid Thalassema melittn,
which burrows on the western shore of
rivers Island.
C. xonczlis, which never accumulates
mesobilivcrdin,
has been found sympatritally only with green C. torquczta populations ( Mangum 1962b). This is, of course,
an empirical generalization
based on a
limited number of observations; future surveys may disclose exceptions. The situation can be interpreted
presently in at
least three ways: 1) Both species ingest
algae or detritus containing the pigment,
but only C. xonalis breaks down and utilizes it. C. torqucltn merely stores it as an
extraneous but harmless by-product.
2)
Both species ingest pigment-containing
material, but C. xon&s returns it to the environment.
3) Only C. torquntn ingests
pigment-containing
material.
The importance of chlorophyll derivatives
in the metabolic economy of Chaetopterus
variopedcztus has been inferred from their
accumulation and continued storage during
prolonged periods of starvation (Kennedy
and Nicol 1959; Rimington and Kennedy
1962). Such an inference is by far the most
tempting
one here, for C. torqunta is
equally tenacious in its storage of mesobiliverdin.
However, the alternative explanations cannot be discarded without
additional evidence.
Since the depth below the substratum
surface from which the two species feed
is not the same, there is no necessity to
postulate different mechanisms of ingestion.
C. xonnlis feeds from 8-15 cm depth, while
C. torquatcz feeds from 20 cm depth. The
depth in both cases may be great enough
to exclude large numbers of living algal
cells, and hence the immediate origin of
mcsobiliverdin
in C. torquntn
may bc
detritus.
C. xor~alis is always outnumbered by C.
torquuta in the sympatric situation.
It
would seem reasonable to suppose that it
can coexist with C. torqunta only when
ECOLOGY
OF MALDANID
the diet of the more successful specks diverges from its own, which is possible in
sediments rich in blue-green algae. But the
more fundamental significance of pigment
accumulation will not become clear until
its metabolism is understood.
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