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Settlement and recruitment patterns of a pedunculate barnacle, Pollicipes polymerus Sowerby, off La Jolla, California
J. Exp. Mar. Biol. Ecol., 1989, Vol. 125, pp. 83-98 Elsevier
83
JEM 01194
Settlement and recruitment patterns of a pedunculate barnacle, Pollicipes polymer-us Sowerby, off La Jolla, California Daniel L. Hoffman Department of Biology, Bucknell University,Lewisburg, Pennsylvania, U.S.A.
(Received 13 April 1988; revision received 12 October 1988; accepted 20 October 1988) Abstract: Settlement of cyprid larvae of Pollicipes polymerus Sowerby on peduncles of adult conspecilics
occurs year-round offthe coast of La Jolla, California, with peak settlement occurring during the early spring months. Spat mortality is relatively high during the first 2-4 wk after settlement. Survival of juveniles reaches maximum levels during the summer months, however, recruitment of juveniles occurs on a yearround basis. Juveniles between 1 and 9 mm rostro-carinal length remain attached to adult peduncles. Juvenile barnacles appear to form peduncular extensions that allow them to reattach to the rocky substratum; above this size range, barnacles tend to be attached directly to the rocky substratum. Growth of Pollicipes in newly established aggregates is quite rapid. Individuals growing on an inverted horizontal surface attained a mean rostro-carinal length of 9 mm in N 1 month. However, on newly exposed vertical surfaces, > 7 months elapsed before the barnacles were able to establish themselves, probably from spat that settled within crevices on the rock surface. Survival from spat to juveniles is highest on solitary adults and lowest in mixed barnacle-mussel aggregates. In addition, recruitment patterns tend to show a greater survival of juveniles at the lower midtidal level. Key words: Growth; Juvenile; Pollicipespolymerus; Recruitment; Settlement
The exposed rocky midtidal zone of the Pacific Coast of North America is characterized by a distinctive epibiota. Ricketts & Calvin (1968) refer to the Mytilus-Pollicipes-Pisaster association as the “horizon markers in marine ecology, typically associated wherever there is a stretch of rocky cliff exposed to the open Pacific”. Primary space, that is, attachment sites on the rocky substratum is often a limiting resource for the mussels and barnacles (Paine, 1966,1974; Dayton, 1971). The most effective competitor for this resource is the sea mussel Mytilus calfimianus; within the midtidal zone, it can sometimes be found in vast numbers, often forming a distinctive monotypic band. The selective foraging behavior of the sea star Pisaster ochraceus sometimes crops back this dominant competitor, and can, thus, be responsible for maintaining high levels of species diversity within the midtidal community (Paine, 1966). Correspondence address: D. L. Hoffman, Department of Biology, Bucknell University, Lewisburg, PA 17837, U.S.A. 0022-0981/89/$03.50 Q 1989 Elsevier Science Publishers B.V. (Biomedical Division)
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D. L. HOFFMAN
The stalked or pedunculate barnacle Pollicipespolymerus Sowerby, the third member of this triumvirate, occurs in distinctive rosette-shaped aggregates at its upper limits of distribution, Lower in the midtidal, the barnacle tends to be interspersed among the vast Mytilus beds, occurring as individuals or aggregates. Paine (1974) reports that on vertical surfaces the barnacles tend to coexist with the mussels, but on horizontal platforms the barnacles are overgrown by the mussels. The aggregative pattern of this barnacle is attributed to the preferential settlement of their cyprid larvae on the peduncles of adult conspecitics (Barnes & Reese, 1960; Lewis, 1975). Apparently, settlem~t on adults affords the juveniles a refuge from predation and desiccation. Although Pollicipes has a broad distribution along the West Coast of North America, the brooding activity indicates two geographically disparate races. The boundary between races corresponds to the cold and warm temperature zones located north and south of Point Conception (Cimberg, 1981). The cross-fertilizing hermaphrodite has a reproductive season correlated with latitude, probably a reflection of the critical air or water temperature (Lewis & Chia, 1981). Near the northern limit of its range, on San Juan Island, Washington, Poll~~~e~is reproductive from April to October (Lewis & Chia, 198 1); near San Francisco, from late March to early January (Hand et al., 1973); in Monterey Bay, from April to December (Hilgard, 1960); and year-round near Santa Barbara (Straughan, 1971; Page, 1986). Pollicipes from northern Washington grows rapidly during its 1st yr attaining rostro-carinal lengths of 18 mm (Paine, 1974; Lewis & Chia, 1981). At Tatoosh Island, Washington, Paine (1974) reports that barnacles achieved rostro-carinal lengths of z 35 mm after 72 months. The largest specimens (with rostro-carinal lengths > 30 mm), however, may be as much as 20 yr old (Barnes & Reese, 1960), although there is no method that can accurately determine their age. Connell (1985) defines settlement as the point when an individu~ first takes up permanent residence on the substratum. In the case of a barnacle, settlement occurs when the larva has cemented itself to a surface. Recruitment, he states further, is a measure of the recently settled juveniles that have survived for a period of time after settlement. There have been few, if any, studies that correlate settlement and recruitment, mainly because larvae are very small when they attach or they do so in cryptic habitats such as on other organisms or in crevices. Once larvae have settled, they are open to mortality. Since the cyprid larvae of Pollicipes tend to settle on the peduncles of conspecifics, both settlement and recruitment can be readily measured. Presently, there is little information concerning the settlement, re~~itment and juvenile growth rates of PoZ~icipes,especially from southern California populations. Hoffman (in press) has shown that the juvenile stages of Pollicipes off La Jolla, California, tend to settle gregariously and grow quite rapidly, especially if they are continuously immersed in flowing seawater. Page (1983) gives evidence that food plays a greater role in influencing estimated production compared to water temperature. Page (1986) further reports that growth and survival rates are greater for adult barnacles in the offshore oil-well platform populations compared to onshore animals. This increase in adult size is attributed to stability of the substratum and an increase in intraspecific competition restricting the
SETTLEMENTAND RECRUITMENTIN POLLICIPES
85
growth of recent recruits. But major questions remain concerning the recruitment of juveniles into adult aggregates. (1) How and where are new aggregates established on the primary substratum, if indeed, the larvae prefer to settle on adults? (2) What are the fates (survival) and growth rates of those recruits that settle into aggregates? Finally, (3) What effect do such factors as size of aggregate and position in the intertidal have on survival and growth of recruits?
MATERIALSAND METHODS SAMPLINGMETHODS Settlement and recruitment of Pollicipes along the La Jolla shoreline were measured from random destructive samples of aggregates taken from three study areas. The destructive sampling method gave an accurate measure of the total number of settled spat and small juveniles hidden within the contracted aggregates. I define spat as those individuals < 1 mm in rostro-car&l (RC) length. All or parts of aggregates were removed from rock and taken to the laboratory where they were disaggregated to facilitate counting and sizing of individuals. All barnacles were sized according to their RC length (after Lewis & Chia, 1981) using a dissection microscope fitted with a calibrated ocular micrometer. Spat < 1 mm RC were pooled into one size class. Most measured ~500 pm in RC length. From my observations in the Scripps Flume (Hoffman, in press), I estimated that these spat were l-3 days old. The mean number of spat per adult barnacle was used as an index of settlement. Recruitment was measured as the number of juvenile barnacles that were attached to an adult substrate. After several months of collecting such data, I decided to use the number of juveniles in the l-9 mm size range, as a measure of recruitment. These juveniles typically were attached to the adult peduncles, while larger animals were generally cemented to the primary substratum. Lewis (pers. comm.) found that barnacles off San Diego are reproductive at 10 mm RC length. STUDYSITES Three areas along the La Jolla shoreline were chosen as study sites. Dike Rock, ~0.4 km north of the Scripps Pier (32”52’ 12” N: 117” 15’ 17” W), is a seawardly sloping rock shelf composed of Miocene Andesite. Large numbers of Pollicipes occur on its seaward face = 0.5-2 m above MLLW. Random samples of barnacles were taken from a 1 x 3-m square quadrant at the 1-1.5-m level above MLLW every 4-6 wk beginning in September 1983 through April 1984; and again from March through September 1985. Settlement rates, recruitment and growth were monitored from sizefrequency data generated from these 4-6 wk samples. Sometime in early November 1983, a large boulder (1.5 x 1.3 x 1.8 m) resting at the edge of an Ardath shale bouldertield was undercut by storm waves exposing its bottom
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D. L. HOFFMAN
to settlement by iUyti1u.sedulis and Pollicipes spat. This was the only site during my field studies in which I observed settlement of barnacle spat directly onto primary substrate and was able to take growth measurements over time. This rock (Barnacle Rock) sits at the edge of the midtidal, x0.5 m above MLLW, and is located 7 km north of the Scripps Pier, near the boundary of Torrey Pines State Reserve (32”54’28” N : 117” 15’23” W). A heterogeneous assemblageofb~acles and mussels established itself on the undersurface of this large rock propped up by neighboring rocks. 3 wk earlier (27 October 1983) the bottom was covered by sand; therefore, I assumed that the initially observed colonists must be no > 3-wk old. From this day (17 November 1983) to 13 April 1984, I destructively sampled 25 x 25-cm quadrants on a monthly basis recording settlement and growth rates each time. The exposed outer surface of the seawall at Children’s Pool served as the third study area, The steel-reinlorced concrete wall, x0.5 km south of the La Jolla Cove (32”50’54” N: 117” 16’36” W) is 4 m high and 120 m in length. The outer surface receives the full force of the surf and is heavily colonized by Pollicipes. Barnacles were sampled to determine the effect of the following parameters on settlement and recruitment: size of aggregates, the presence of mussels within the aggregates, and the relative position of the aggregate on the sea wall (height of tidal exposure). Barnacles were sampled beginning January 1984 and intermitten~y until March 1987. In order to determine the effect of aggregate size on the settlement and rec~~ent of juveniles, I took the following barnacle samples at the seawall: solitary or isolated adult barnacles, 4-10 adults * aggregate- I, and 2 20 adults ’ aggregate- i. To determine if the relative position of the barnacles above MLLW within the intertidal had any effect on settlement and recruitment or survival of juveniles, aggregates of equivalent size were taken randomly along a transect line drawn from 2 m above MLLW to the lower midtidal, *O-O.5 m above MLLW. RECRUITMENT
EXPERIMENT
Two vertical-facing rock surfaces z 1 x 0.75 m (0.5-1.5 m above MLLW) bearing a mixed population of barnacles and mussels were scraped clean of all organisms in order to study the successional events involved in the natural establishment of Pollicipes on rocky substrata. The rocks were located on the seaward edge of an Ardath shale ~ulde~eld z 50 m north of Barnacle Rock. The given areas were scraped clean of all organisms on 5 October 1983 and the surfaces were examined monthly until May 1984. I returned during March 1985 to make a final observation. I kept a record of the sequence of organisms that recolonized these cleared surfaces. The ambient water temperature along the La Jolla shoreline ranged from a high of 20 “C in September 1983 to a low of 15.5 “C in January 1984.
SETTLEMENT
AND RECRUITMENT
87
IN POLLICIPES
RESULTS
SETTLEMENT Spats
AND RECRUITMENT
OF POLLICIPES INTO AGGREGATES
< 1 mm in RC length from
all aggregates
sampled
on Dike
Dock
were found
year-round (Table I). In most cases, settlement was limited to the peduncles, especially that region proximal to the capitulum. The largest number of such recent recruits was TABLE I Spat settlement
and recruitment
of juveniles
Date
Number of adults > 9 mm RC length
Sep 1983 Ott Nov Dee Jan 1984 Feb Mar
121 102 71 77 44 104 52 42 55 69 60 30
Apr Mar 1985 May JUl Sep
into aggregates California.
from Dike Rock,
ji number of spat (O-1 mm RC) . adult barnacle- ’ k SE 13.95 21.60 8.14 14.40 9.05 11.34 74.00 133.29 290.42 49.97 40.93 21.03
+ + f f f & f f f + f f
Scripps
Beach,
La Jolla,
X number of juveniles (1-9 mm RC) adult barnacle’ + SE
2.17 2.96 1.41 1.34 1.21 1.31 6.66 9.29 14.32 6.27 3.59 3.96
5.46 0.54 0.96 1.54 1.09 0.37 0.93 1.74 0.55 0.42 4.10 0.79
+ 0.59 f 0.12 f 0.23 + 0.31 _+0.18 * 0.07 * 0.15 + 0.36 * 0.13 f 0.11 * 1.05 + 0.19
observed in April 1984 and again in March 1985. In the first case, ~25% of the barnacles > 10 mm bore 2200 recently settled spat. During March of the following year, 60% of the barnacles > 9 mm carried spat in excess of 300 * individual - ’ ; one adult individual (RC length 23 mm) bore 1260 spat on its peduncle. Large numbers of cyprid larvae were found among the recently settled, metamorphosed spat during these peak periods, but their numbers were not counted since many were not fully attached. Typically, the spat and juveniles clustered on the proximal section of the peduncle just under the rostrum or carina of the capitulum. The number of juveniles reached maximum levels during the summer months evidenced by large numbers of juveniles < 10 mm during those samples taken in September 1983 and July 1984 (Table I). However, on an average, at least one juvenile could be found per adult on those months that counts were made. ESTABLISHMENT
AND GROWTH
OF POLLICZPES ON NEWLY
AVAILABLE
ROCKY
SUBSTRATUM Size-frequency distributions of Pollicipes juveniles taken from the undersurface of Barnacle Rock are given (Fig. 1). Within x 1 month of establishment (November 1983),
88
D. L. HOFFMAN
animals > 9 mm RC length comprised > 50% of the total population. These larger barnacles were attached directly to the rock. By March 1984, a definite bimodality becomes apparent that is similar to longer established aggregates on vertical surfaces.
60
50
40
30 MAR
APR
84
84
% 20
10
r-l
Fig. 1. Size-frequency distributions of recently settled juveniles from Barnacle Rock.
Mean growth of these barnacles over 5 months is shown (Fig. 2). By April, the mean size of those animals attached to the primary substratum approaches 15 mm. Each bare section of rock that was cleared by sampling was recolonized by some barnacles and mussels within 1 month. Different sections of the undersurface of the rock were sampled
SETI-LEMENT AND RECRUITMENT IN POLLICIPES
89
to follow the natural barnacle growth. There was no evidence at this site that the barnacles settled on mussel shells; either they settled directly to rock surface or, in the case of the smallest size classes (O-9 mm RC length), to the peduncles of larger animals.
I I I 1 NO~DE~‘JAN’FEB
t
!
‘MAR APR
Fig. 2. Mean growth curve of Pollicipes on Barnacle Rock from November 1983 through April 1984. Mean length given in millimeters RC length f SD.
SETTLEMENT AND RECRUITMENT AT LA JOLLA SEAWALL
The population structure of Po~l~c~eson the seawall relative to tidal exposure was sampled during March 1985 (Fig. 3). At high midtidal (2 m above MLLW), the curve is bimodal with 52% of the barnacles 2 10 mm RC length and no adults were > 19 mm. Within the midtidal range (Z l-l .5 above MLLW), the population curve changes with 29% of the population comprised of adult barnacles (> 9 mm RC length), At the lower limit of the midtidal zone, where barnacles were interspersed among mussels (0.5-l m above MLLW), the population again becomes bimodal, with 28 % > 9 mm in RC length. Larger adults, > 18 mm RC length, comprise 18% of the total population. The settlement and recruitment of Pollicipes as a function of tidal exposure (March 1985) is given (Table XI).There is no difference in the settlement patterns (mean number of attached spat - barnacle- i), however, the recruitment patterns tend to show a greater survival of juveniles in the l-9 mm class at the lower midtidal level. The relationships between spat settlement and juvenile survival (recruitment) and the size of established aggregates (March 1985) are given (Table III). There is a positive relationship between the size of the aggregate and spat settlement. Recruitment and juvenile su~ivorship is also a function of aggregate size where the percent survival of juveniles is greater on the solitary barnacles than on the larger mixed barnacle-mussel aggregates. RECRUITMENT
EXPERIMENT
Excluding encrusting algae and diatoms, the initial colonizers of the denuded vertical rock surfaces were spat of the barnacle ~hthffrnal~s~~~ which first appeared during late January 1984. By May of the same year, no mussels or Pollicipes had established
D. L. HOFFMAN
90
SIZE
25
20.
15.
MID
% 101
5.
5
10
SILL
15
20
SETTLEMENT
AND RECRUITMENT
91
IN POLLICIPES
TABLE II Spat
settlement
of Policipes off La Jolla, (March 1985).
and recruitment
California,
as a function
of tidal
exposure
Position
n
X number of spat + SE adult barnacle _ ’
X number of recruits + SE adult barnacle - ’
High midtidal 2 m above MLLW Midtidal l-l.5 m above MLLW Low midtidal 0.5 m above MLLW
135
22.36 f 2.33
0.51 & 0.09
96
45.89 f 4.91
0.64 f 0.10
60
33.1 f 3.36
7.07 +_ 1.10
TABLE III Relationship
between
spat
Type of assemblage
settlement
n
and recruitment of juveniles (March1985). X number of Spat 2 SE adult barnacle -
’
and size of barnacle
2 number of juveniles + SE adult barnacle -
aggregation
y0 Survival from spat to juvenile
’
Solitary adults Very small aggregate (4-10. aggregate‘) Small aggregate (20-30. aggregate‘)
51 73
8.2 + 16.48 k
3.5 1.84
0.99 f 0.45 0.59 f 0.31
12.1 3.6
56
25.50 +
3.64
2.63 f 1.40
10.3
Mytilus-Pollicipes
52
3.95 f 1.51
3.1
105.90 & 12.951
mixed aggregate
themselves in these open areas. I was not able to return to these rocks until March 1985. At that time, a mixed band ofMyti1u.rcalijGmianus and Pollicipes had become established on the surfaces (Fig. 4). Destructive samples of this assemblage were compared to an assemblage at the same tidal level from the La Jolla seawall to determine differences in settlement and recruitment rates (Table IV). By this date, 17 months after initiating the experiment, adults > 15 mm RC length were found. 33 % of the adults > 10 mm had in excess of 200 spat attached to their peduncles. Recruitment rates were high and compared favorably with aggregates taken at the same tidal level on the seawall.
Fig. 3. Size-frequency distributions of population structures of Pollicipes at three different tidal levels on Children’s Pool seawall (March 1985). HIGH, 2 m above MLLW; MID, l-5 m above MLLW; LOW, 0.5 m above MLLW.
92
D. L. HOFFMAN
*1
93
SETTLEMENT AND RECRUITMENT IN POLLICIPES TABLE IV
Spat
settlement
Location
Recolonized rock La Jolla seawall
and
recruitment
n
37 52
of juveniles into recolonized (March 1985).
barnacle-mussel
assemblage
X number of spat + SE adult barnacle- ’
.iE number of recruits & SE
140.68 & 14.56 105.90 + 12.95
6.00 + 1.28 3.95 & 1.47
*adult bamacie - ’
DISCUSSION Pa~lic~es grow rapidly off La Jolla, at least in newly established aggregates. Spat
under Barnacle Rock grew at the mean rate of = 9 mm RC length in z 1 month after settlement. The barnacles invariably remained protected from desiccation on the inverted horizontal surface beneath the rock and received food from the surging water that had undercut the rock. Previously, I showed that under the artificial constraints of total submergence in fast-flowing aerated water in the Scripps intake seawater system Pollicipes could grow quite rapidly reaching a mean size of 4 mm in just 28 days (Hoffman, in press). However, these measurements included spat (O-l mm RC length) which lowered the mean size of the sample. Such rapid growth rates for pedunculate barnacles have been reported in other species. Macintyre (1966) reported that the opportunistic Lepas anatifera and Conchoderma virgata require from 17 and 50 days, respectively, to reach reproductive size in tropical waters. 17 days after a newly painted marker buoy was laid off the east coast of Australia, reproductive specimens of Lepas 23 mm capitular length were measured. Most measurements of Pollicipes indicate that the growth of the barnacle averages 1.2 mm * month- ’ (Paine, 1974), but these data were collected from barnacles growing in already well established aggregates. Page (1986) demonstrated that interspecific pressure exerted by the larger adults may inhibit the growth of smaller juveniles in such aggregations. Along the coastline of La Jolla, Pollicipes settles year-round on the peduncles of conspecifics with peak settlement beginning in the early spring (March-April). At this time, the larvae tend to settle in aggregative pattern at the proximal end of the peduncle just under the rostra1 and carinal margins of the capituium. This proximal end of the peduncle is a zone of growth producing new cuticle which may be attracting settling larvae (Darwin, 1851; Hoffman, 1984). Also this region of the animal is not in contact with adjacent barnacles and affords an exposed attachment surface. The density of
Fig. 4. Recruitment experiment. (A) Vertical seaward-facing rock with 0.75 x 1m area denuded (scraped) of all macroscopic organisms (October 1983). Note crack or fissure in rock (arrow). (B) Same rock surface on March 1985 colonized by ~ytil~ and PolZkzpes.(C) Close-up photo~aph of new P~~l~c~~es-~~i~l~s assemblages along fissure area of rock.
94
D. L. HOFFMAN
recently settled spat can be remarkable, > 300 * cm - ’ cm of peduncular surface. More accurate settlement rates could have been defined if the mean number of spat per unit area of stalk surface were determined. However, such determinations proved to be very difficult to make since the spat were patchily distributed on the peduncles. Usually, the spat were just proximal to the rostrum and carina. Also, the surface area of adult peduncles is not directly proportional to the RC length. Often, large adults with relatively large peduncular surface areas would house few or no spat. The reason for these variations is not known. Many of the larger and obviously older barnacles often have epiphytic algae attached to their peduncles which may impede larval settlement. Rarely, if ever, are young spat observed on any of the capitular plates. However, when adults are constantly immersed in running seawater (the Scripps seawater system), cyprid larvae do settle on the capitular plates and valves and grow into juveniles (Hoffman, in press). This indicates that the distribution of juveniles on adults may be due in part to their ability to withstand desiccation. During the months that these observations and measurements were taken, there was little evidence that Pollicipes cyprid larvae were establishing new aggregates on open hard substrates, excluding the underside of Barnacle Rock. The rocky surfaces adjacent to established aggregates were scrupulously examined with a magnifying glass on each monthly data collecting trip. On 2 September 1983, what appeared to be a newly established aggregate (2 x 6 cm) was observed along a rock fissure at the 0.5 m MLLW level. Small juveniles (the largest measuring 6 mm RC length) comprised this aggregate. However, 2 days later, the aggregate had been obliterated by beach sand, apparently smothering the barnacles. The recolonization of denuded vertical facing boulders by Pollicipes took in excess of 7 months which tends to run contrary to what occurred under Barnacle Rock. This difference may be explained by the orientation and exposure of the substrata. At Barnacle Rock, the settlement area was the horizontal undersurface of a rock, relatively protected from desiccation. The denuded rocks were seaward facing vertical surfaces, exposed to the drying rays of the sun at low tide, Settlement probably occurred at some time during the summer months. Inferred from the position of the barnacle aggregates (Fig. 4), initial settlement may have begun in a small crevice that ran along the face of the boulder. The survivors served as founders that attracted other barnacle settlers. Mortality during the fust 2-3 wk after settlement is relatively high in PoZIicipesspat. Connell (1961) suggested that mortality of ~e~ib~Zunu~ b~~~noi~esduring settlement periods was independent of settlement density and may be due to such physical factors as storms and periods of dry weather. Although I have no experimental evidence regarding the cause of this high mortality, there is observational evidence that it may be due in part to their position in the intertidal zone. During winter storms and also during hot dry periods of low tide exposure, mortality may be quite high. In addition, much sand and surf grass debris was usually embedded between or wrapped around the peduncles. These inclusions, in association with rows of minute cdcareous peduncular spines may have abrasive action on the spat and juveniles. Finally,
SE~LEME~
AND RECRUITMENT
IN
POLLICIP~~
95
numerous species of invertebrates within the aggregates may affect mortality. I observed on at least six occasions the nemertean Emplectonema gracile apparently foraging on small juveniles (1 mm RC length). The worms often were wrapped around small juveniles, many of which lacked capitula. Large numbers of polyclad flatworms, crabs, amphipods, and opisthobranch mollusks, all possible predators of young animals, also reside within the barnacle aggregates. Restriction in growth rates and survival of recent recruits of Pollici~es also is reportedly due to competition between the estab~shed adults and the recruits for food resources (Page, 1986). When large adults were expe~ment~ly removed from an aggregate, the smaller barnacles were able to increase rapidly in size. Page postulates that the large barnacles may interfere with the water flow that brings food to the smaller barnacles. In the mussel M’tilus edulis, Kantsky (1982) also reported that growth was suppressed in small mussels by increased density of large mussels. There appears to be a correlation between survival of recruits and the position of the recruits within the intertidal (Table II). The settlement rates of spat as a function of tidal position is consistent, indicating that the survival of the recruits may be independent of settlement density. However, juvenile survival also tends to be variable and dependent on clump size (Table III). The percent survival of juveniles is high on solitary barnacles which are encountered throughout their vertical distribution. Even though settlement is relatively sparse, recruitment is high. Whether or not these solitary barnacles serve as founders of new aggregates could not be determined during the course of these studies, however, Lewis (pers. comm.) indicates that such solitary adults may represent remnants of destroyed aggregates. Connell (1961, 1970) has demonstrated in acorn barnacles that predation plays an important role in recruit survival at their lower intertidal limit. In the lower levels of its dist~bution, Pollicipes is typically associated with mussels, either M. cu~~~~ianu~or M. edulis. Although the interaction between barnacles and mussels has been reported to be highly competitive for space, there may be positive value afforded by this relationship to the barnacle. In a homogeneous barnacle assemblage, there is little space between the peduncles for juveniles to attach to the primary substratum. However, in a mixed barnacle-mussel assemblage, the convex shells of the bivalves disrupt the space available to the larger adult barnacles affording room for the smaller juvenile recruits. When a section of barnacle-mussel assemblage is lifted off the substratum, large numbers of small Pollicipes (RC lengths < 6 mm) can be found attached directly to the substratum. Is it m~adaptive for Po~Zicipeslarvae to settle on the peduncles of conspeci~cs? These data indicate that barnacles with RC lengths > 9 mm are attached to the rocky substratum, whereas those below this size class tend to be attached to adults. In previous papers (Hoffman, 1981, 1984), I gave indirect evidence that the juveniles of Pollicipes may have limited mobilities by producing peduncular extensions at the distal end of the peduncle which seeks and attaches to the primary substratum. Within barnacle aggregates, many juveniles (RC lengths of I9 mm) may be found with these rhizoid-like processes extending downward from the adult peduncle (Fig. 5). The distal end of the
96
D. L. HOFFMAN
peduncle apparently also can give rise to new cuticle (ChatTee & Lewis, 1988). The circulatory pressure within the peduncle is reportedly one ofthe highest in the Crustacea, as high as 33 km. mm2 (Crenshaw, 1979; B. Burnett, pers. comm.). These high pedun-
Fig. 5. Juvenile Pollicipes(6 mm RC length) attached to peduncle of adult Pollicipes( 14 mm RC length). Note light-colored peduncular extension forming from distal end ofjuvenile peduncle. In living specimens, these extensions appear bright red due to thinness of cuticle and hemoglobin contained within.
cular pressures in association with cuticular growth zones might be used in association not only to extend the capitulum upward when feeding and during copulation between adults, but also to thrust the newly formed extension downward to find a new attachment site. These extensions also appear to carry ducts from the cement glands that adhere them to a new site on the primary substratum (pers. obs.). Therefore, preferential attachment of larvae on conspecifics may be highly adaptive to the surviving recruits,
SETTLEMENT
AND RECRUITMENT
IN POLLICIPES
91
for not only does it afford initial survival value for the fragile spat against desiccation, but also serves as an effective conduit that allows their eventual attachment to the primary substratum.
ACKNOWLEDGEMENTS
I thank W. A. Newman, P. K. Dayton, J. Barry, R. McConnaughey and B. Burnett for their help with this project. To C. A. Lewis and two anonymous reviewers, my thanks for their critical review of this paper. I also thank my wife Marcia and sons Noah and Tyler. This research was supported in part by a grant from the National Science Foundation, OCE-8 120943, and a faculty development grant from Bucknell University.
REFERENCES Barnes, H. & E. S. Reese, 1960. The behavior of the stalked intertidal barnacle Pollicipes polymerus J.B. Sowerby, with special reference to its ecology and distribution. J. Anim. Ecol., Vol. 29, pp. 169-185. Chaffee, J. & C.A. Lewis, 1988. Pendunculate barnacle stalk growth. J. Exp. Mar. Biol. Ecol., Vol. 124, pp. 145-162. Cimberg, R.L., 1981. Variability in brooding activity in the stalked barnacle, Pollicipespolymerus. Biol. Bull., (Woods Hole, Muss. ), Vol. 160, pp. 31-42. Connell, J. H., 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology, Vol. 42, pp. 710-723. Connell, J.H., 1970. The predator-prey system in the marine intertidal region. I. Balunus glandula and several species of Thaic. Ecol. Monogr., Vol. 40, pp. 49-78. Connell, J. H., 1985. The consequences ofvariation in initial settlement vs. post-settlement mortality in rocky intertidal communities. J. Exp. Mar. Biol. Ecol., Vol. 93, pp. 1 l-45. Crenshaw, D.G., 1979. Hydrostatic support of the pedunculate barnacles, Pollicipes polymerus. Comp. Biochem. Physiol., Vol. 62A, pp. 423-425. Darwin, C., 1851. A monograph on the class Cirripedia, with figures of all species. The Lepadidae; or pedunculate cirripedes. The Ray Society, London, 400 pp. Dayton, P. K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 35 l-389. Hand, C., J.D. Standing & J.C. Rutherford, 1973. San Francisco oil spill, effects on reproduction in intertidal invertebrates (Project No. 15080). U.S. Environmental Protection Agency, Washington, DC., 46 PP. Hilgard, G. H., 1960. A study of reproduction in the intertidal barnacle, Mitellapolymerus, in Monterey Bay, California. Biol. Bull. (Woods Hole, Muss.), Vol. 119, pp. 169-188. Hoffman, D.L., 1981. Foot-loose barnacles: implication of the retention of mobility into the postmetamorphic stages of the goose barnacle. Am. Zool., Vol. 21, p. 969 (abstract). Hoffman, D. L., 1984. Size-frequency distribution patterns ofthe juvenile stages ofthe pedunculate barnacle, Pollicipes polymerus Sowerby, 1833 (Cirripedia, Lepadomorpha). Crustaceana (Leiden), Vol. 46, pp. 295-299. Hoffman, D.L., in press. Settlement and growth of the pedunculate barnacle, Pollkzpespolymencs Sowerby, in an intake seawater system at the Scripps Institution of Oceanography, La Jolla, California. Pact? Sci. Kantsky, N., 1982. Growth and size structure in a Baltic Myrilus edulis population. Mar. Biol., Vol. 68, pp. 117-133. Lewis, C. A., 1975. Some observations on factors affecting embryonic and larval growth of Pollicipes polymerus (Cirripedia, Lepadomorpha) in vitro. Mar. Biol., Vol. 32, pp. 127-139. Lewis, C. A. & F.-S. Chia, 1981. Growth, fecundity and reproductive biology in the pedunculate cirripede,
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Pollicipes polymerus at San Juan Island, Washington. Can. J. Zool., Vol. 59, pp. 893-901. Macintyre, R. J., 1966. Rapid growth in pedunculate barnacles. Nature (London), Vol. 5062, pp. 637-638. Page, H.M., 1983. Effect of water temperature and food on energy allocation in the stalked barnacle, Pollicipespolymerus Sowerby. J. Exp. Mar. Biol. Ecol., Vol. 69, pp. 189-202. Page, H.M., 1986. Differences in population structure and growth rate of the stalked barnacle Pollicipes polymerus between a rocky headland and an offshore oil platform. Mar. Ecol. Prog. Ser., Vol. 29, pp. 157-164. Paine, R.T., 1966. Food web complexity and species diversity. Am. Nat., Vol. 100, pp. 65-75. Paine, R.T., 1974. Intertidal community structure. Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia (Berlin), Vol. 15, pp. 93-120. Ricketts, E. F. & J. Calvin, 1968. Between Pacific tides (revised by J. W. Hedgpeth). Stanford University Press, Stanford, California, 614 pp. Straughan, D., 1971. Breeding and larval settlement of certain intertidal invertebrates in the Santa Barbara Channel following pollution by oil. In, Biological and oceanographic survey of the Santa Barbara oil spill 1969-1970, Vol. I, edited by D. Straughan, Allan Hancock Foundation, University of Southern California, Los Angeles, pp. 223-244.
83
JEM 01194
Settlement and recruitment patterns of a pedunculate barnacle, Pollicipes polymer-us Sowerby, off La Jolla, California Daniel L. Hoffman Department of Biology, Bucknell University,Lewisburg, Pennsylvania, U.S.A.
(Received 13 April 1988; revision received 12 October 1988; accepted 20 October 1988) Abstract: Settlement of cyprid larvae of Pollicipes polymerus Sowerby on peduncles of adult conspecilics
occurs year-round offthe coast of La Jolla, California, with peak settlement occurring during the early spring months. Spat mortality is relatively high during the first 2-4 wk after settlement. Survival of juveniles reaches maximum levels during the summer months, however, recruitment of juveniles occurs on a yearround basis. Juveniles between 1 and 9 mm rostro-carinal length remain attached to adult peduncles. Juvenile barnacles appear to form peduncular extensions that allow them to reattach to the rocky substratum; above this size range, barnacles tend to be attached directly to the rocky substratum. Growth of Pollicipes in newly established aggregates is quite rapid. Individuals growing on an inverted horizontal surface attained a mean rostro-carinal length of 9 mm in N 1 month. However, on newly exposed vertical surfaces, > 7 months elapsed before the barnacles were able to establish themselves, probably from spat that settled within crevices on the rock surface. Survival from spat to juveniles is highest on solitary adults and lowest in mixed barnacle-mussel aggregates. In addition, recruitment patterns tend to show a greater survival of juveniles at the lower midtidal level. Key words: Growth; Juvenile; Pollicipespolymerus; Recruitment; Settlement
The exposed rocky midtidal zone of the Pacific Coast of North America is characterized by a distinctive epibiota. Ricketts & Calvin (1968) refer to the Mytilus-Pollicipes-Pisaster association as the “horizon markers in marine ecology, typically associated wherever there is a stretch of rocky cliff exposed to the open Pacific”. Primary space, that is, attachment sites on the rocky substratum is often a limiting resource for the mussels and barnacles (Paine, 1966,1974; Dayton, 1971). The most effective competitor for this resource is the sea mussel Mytilus calfimianus; within the midtidal zone, it can sometimes be found in vast numbers, often forming a distinctive monotypic band. The selective foraging behavior of the sea star Pisaster ochraceus sometimes crops back this dominant competitor, and can, thus, be responsible for maintaining high levels of species diversity within the midtidal community (Paine, 1966). Correspondence address: D. L. Hoffman, Department of Biology, Bucknell University, Lewisburg, PA 17837, U.S.A. 0022-0981/89/$03.50 Q 1989 Elsevier Science Publishers B.V. (Biomedical Division)
84
D. L. HOFFMAN
The stalked or pedunculate barnacle Pollicipespolymerus Sowerby, the third member of this triumvirate, occurs in distinctive rosette-shaped aggregates at its upper limits of distribution, Lower in the midtidal, the barnacle tends to be interspersed among the vast Mytilus beds, occurring as individuals or aggregates. Paine (1974) reports that on vertical surfaces the barnacles tend to coexist with the mussels, but on horizontal platforms the barnacles are overgrown by the mussels. The aggregative pattern of this barnacle is attributed to the preferential settlement of their cyprid larvae on the peduncles of adult conspecitics (Barnes & Reese, 1960; Lewis, 1975). Apparently, settlem~t on adults affords the juveniles a refuge from predation and desiccation. Although Pollicipes has a broad distribution along the West Coast of North America, the brooding activity indicates two geographically disparate races. The boundary between races corresponds to the cold and warm temperature zones located north and south of Point Conception (Cimberg, 1981). The cross-fertilizing hermaphrodite has a reproductive season correlated with latitude, probably a reflection of the critical air or water temperature (Lewis & Chia, 1981). Near the northern limit of its range, on San Juan Island, Washington, Poll~~~e~is reproductive from April to October (Lewis & Chia, 198 1); near San Francisco, from late March to early January (Hand et al., 1973); in Monterey Bay, from April to December (Hilgard, 1960); and year-round near Santa Barbara (Straughan, 1971; Page, 1986). Pollicipes from northern Washington grows rapidly during its 1st yr attaining rostro-carinal lengths of 18 mm (Paine, 1974; Lewis & Chia, 1981). At Tatoosh Island, Washington, Paine (1974) reports that barnacles achieved rostro-carinal lengths of z 35 mm after 72 months. The largest specimens (with rostro-carinal lengths > 30 mm), however, may be as much as 20 yr old (Barnes & Reese, 1960), although there is no method that can accurately determine their age. Connell (1985) defines settlement as the point when an individu~ first takes up permanent residence on the substratum. In the case of a barnacle, settlement occurs when the larva has cemented itself to a surface. Recruitment, he states further, is a measure of the recently settled juveniles that have survived for a period of time after settlement. There have been few, if any, studies that correlate settlement and recruitment, mainly because larvae are very small when they attach or they do so in cryptic habitats such as on other organisms or in crevices. Once larvae have settled, they are open to mortality. Since the cyprid larvae of Pollicipes tend to settle on the peduncles of conspecifics, both settlement and recruitment can be readily measured. Presently, there is little information concerning the settlement, re~~itment and juvenile growth rates of PoZ~icipes,especially from southern California populations. Hoffman (in press) has shown that the juvenile stages of Pollicipes off La Jolla, California, tend to settle gregariously and grow quite rapidly, especially if they are continuously immersed in flowing seawater. Page (1983) gives evidence that food plays a greater role in influencing estimated production compared to water temperature. Page (1986) further reports that growth and survival rates are greater for adult barnacles in the offshore oil-well platform populations compared to onshore animals. This increase in adult size is attributed to stability of the substratum and an increase in intraspecific competition restricting the
SETTLEMENTAND RECRUITMENTIN POLLICIPES
85
growth of recent recruits. But major questions remain concerning the recruitment of juveniles into adult aggregates. (1) How and where are new aggregates established on the primary substratum, if indeed, the larvae prefer to settle on adults? (2) What are the fates (survival) and growth rates of those recruits that settle into aggregates? Finally, (3) What effect do such factors as size of aggregate and position in the intertidal have on survival and growth of recruits?
MATERIALSAND METHODS SAMPLINGMETHODS Settlement and recruitment of Pollicipes along the La Jolla shoreline were measured from random destructive samples of aggregates taken from three study areas. The destructive sampling method gave an accurate measure of the total number of settled spat and small juveniles hidden within the contracted aggregates. I define spat as those individuals < 1 mm in rostro-car&l (RC) length. All or parts of aggregates were removed from rock and taken to the laboratory where they were disaggregated to facilitate counting and sizing of individuals. All barnacles were sized according to their RC length (after Lewis & Chia, 1981) using a dissection microscope fitted with a calibrated ocular micrometer. Spat < 1 mm RC were pooled into one size class. Most measured ~500 pm in RC length. From my observations in the Scripps Flume (Hoffman, in press), I estimated that these spat were l-3 days old. The mean number of spat per adult barnacle was used as an index of settlement. Recruitment was measured as the number of juvenile barnacles that were attached to an adult substrate. After several months of collecting such data, I decided to use the number of juveniles in the l-9 mm size range, as a measure of recruitment. These juveniles typically were attached to the adult peduncles, while larger animals were generally cemented to the primary substratum. Lewis (pers. comm.) found that barnacles off San Diego are reproductive at 10 mm RC length. STUDYSITES Three areas along the La Jolla shoreline were chosen as study sites. Dike Rock, ~0.4 km north of the Scripps Pier (32”52’ 12” N: 117” 15’ 17” W), is a seawardly sloping rock shelf composed of Miocene Andesite. Large numbers of Pollicipes occur on its seaward face = 0.5-2 m above MLLW. Random samples of barnacles were taken from a 1 x 3-m square quadrant at the 1-1.5-m level above MLLW every 4-6 wk beginning in September 1983 through April 1984; and again from March through September 1985. Settlement rates, recruitment and growth were monitored from sizefrequency data generated from these 4-6 wk samples. Sometime in early November 1983, a large boulder (1.5 x 1.3 x 1.8 m) resting at the edge of an Ardath shale bouldertield was undercut by storm waves exposing its bottom
86
D. L. HOFFMAN
to settlement by iUyti1u.sedulis and Pollicipes spat. This was the only site during my field studies in which I observed settlement of barnacle spat directly onto primary substrate and was able to take growth measurements over time. This rock (Barnacle Rock) sits at the edge of the midtidal, x0.5 m above MLLW, and is located 7 km north of the Scripps Pier, near the boundary of Torrey Pines State Reserve (32”54’28” N : 117” 15’23” W). A heterogeneous assemblageofb~acles and mussels established itself on the undersurface of this large rock propped up by neighboring rocks. 3 wk earlier (27 October 1983) the bottom was covered by sand; therefore, I assumed that the initially observed colonists must be no > 3-wk old. From this day (17 November 1983) to 13 April 1984, I destructively sampled 25 x 25-cm quadrants on a monthly basis recording settlement and growth rates each time. The exposed outer surface of the seawall at Children’s Pool served as the third study area, The steel-reinlorced concrete wall, x0.5 km south of the La Jolla Cove (32”50’54” N: 117” 16’36” W) is 4 m high and 120 m in length. The outer surface receives the full force of the surf and is heavily colonized by Pollicipes. Barnacles were sampled to determine the effect of the following parameters on settlement and recruitment: size of aggregates, the presence of mussels within the aggregates, and the relative position of the aggregate on the sea wall (height of tidal exposure). Barnacles were sampled beginning January 1984 and intermitten~y until March 1987. In order to determine the effect of aggregate size on the settlement and rec~~ent of juveniles, I took the following barnacle samples at the seawall: solitary or isolated adult barnacles, 4-10 adults * aggregate- I, and 2 20 adults ’ aggregate- i. To determine if the relative position of the barnacles above MLLW within the intertidal had any effect on settlement and recruitment or survival of juveniles, aggregates of equivalent size were taken randomly along a transect line drawn from 2 m above MLLW to the lower midtidal, *O-O.5 m above MLLW. RECRUITMENT
EXPERIMENT
Two vertical-facing rock surfaces z 1 x 0.75 m (0.5-1.5 m above MLLW) bearing a mixed population of barnacles and mussels were scraped clean of all organisms in order to study the successional events involved in the natural establishment of Pollicipes on rocky substrata. The rocks were located on the seaward edge of an Ardath shale ~ulde~eld z 50 m north of Barnacle Rock. The given areas were scraped clean of all organisms on 5 October 1983 and the surfaces were examined monthly until May 1984. I returned during March 1985 to make a final observation. I kept a record of the sequence of organisms that recolonized these cleared surfaces. The ambient water temperature along the La Jolla shoreline ranged from a high of 20 “C in September 1983 to a low of 15.5 “C in January 1984.
SETTLEMENT
AND RECRUITMENT
87
IN POLLICIPES
RESULTS
SETTLEMENT Spats
AND RECRUITMENT
OF POLLICIPES INTO AGGREGATES
< 1 mm in RC length from
all aggregates
sampled
on Dike
Dock
were found
year-round (Table I). In most cases, settlement was limited to the peduncles, especially that region proximal to the capitulum. The largest number of such recent recruits was TABLE I Spat settlement
and recruitment
of juveniles
Date
Number of adults > 9 mm RC length
Sep 1983 Ott Nov Dee Jan 1984 Feb Mar
121 102 71 77 44 104 52 42 55 69 60 30
Apr Mar 1985 May JUl Sep
into aggregates California.
from Dike Rock,
ji number of spat (O-1 mm RC) . adult barnacle- ’ k SE 13.95 21.60 8.14 14.40 9.05 11.34 74.00 133.29 290.42 49.97 40.93 21.03
+ + f f f & f f f + f f
Scripps
Beach,
La Jolla,
X number of juveniles (1-9 mm RC) adult barnacle’ + SE
2.17 2.96 1.41 1.34 1.21 1.31 6.66 9.29 14.32 6.27 3.59 3.96
5.46 0.54 0.96 1.54 1.09 0.37 0.93 1.74 0.55 0.42 4.10 0.79
+ 0.59 f 0.12 f 0.23 + 0.31 _+0.18 * 0.07 * 0.15 + 0.36 * 0.13 f 0.11 * 1.05 + 0.19
observed in April 1984 and again in March 1985. In the first case, ~25% of the barnacles > 10 mm bore 2200 recently settled spat. During March of the following year, 60% of the barnacles > 9 mm carried spat in excess of 300 * individual - ’ ; one adult individual (RC length 23 mm) bore 1260 spat on its peduncle. Large numbers of cyprid larvae were found among the recently settled, metamorphosed spat during these peak periods, but their numbers were not counted since many were not fully attached. Typically, the spat and juveniles clustered on the proximal section of the peduncle just under the rostrum or carina of the capitulum. The number of juveniles reached maximum levels during the summer months evidenced by large numbers of juveniles < 10 mm during those samples taken in September 1983 and July 1984 (Table I). However, on an average, at least one juvenile could be found per adult on those months that counts were made. ESTABLISHMENT
AND GROWTH
OF POLLICZPES ON NEWLY
AVAILABLE
ROCKY
SUBSTRATUM Size-frequency distributions of Pollicipes juveniles taken from the undersurface of Barnacle Rock are given (Fig. 1). Within x 1 month of establishment (November 1983),
88
D. L. HOFFMAN
animals > 9 mm RC length comprised > 50% of the total population. These larger barnacles were attached directly to the rock. By March 1984, a definite bimodality becomes apparent that is similar to longer established aggregates on vertical surfaces.
60
50
40
30 MAR
APR
84
84
% 20
10
r-l
Fig. 1. Size-frequency distributions of recently settled juveniles from Barnacle Rock.
Mean growth of these barnacles over 5 months is shown (Fig. 2). By April, the mean size of those animals attached to the primary substratum approaches 15 mm. Each bare section of rock that was cleared by sampling was recolonized by some barnacles and mussels within 1 month. Different sections of the undersurface of the rock were sampled
SETI-LEMENT AND RECRUITMENT IN POLLICIPES
89
to follow the natural barnacle growth. There was no evidence at this site that the barnacles settled on mussel shells; either they settled directly to rock surface or, in the case of the smallest size classes (O-9 mm RC length), to the peduncles of larger animals.
I I I 1 NO~DE~‘JAN’FEB
t
!
‘MAR APR
Fig. 2. Mean growth curve of Pollicipes on Barnacle Rock from November 1983 through April 1984. Mean length given in millimeters RC length f SD.
SETTLEMENT AND RECRUITMENT AT LA JOLLA SEAWALL
The population structure of Po~l~c~eson the seawall relative to tidal exposure was sampled during March 1985 (Fig. 3). At high midtidal (2 m above MLLW), the curve is bimodal with 52% of the barnacles 2 10 mm RC length and no adults were > 19 mm. Within the midtidal range (Z l-l .5 above MLLW), the population curve changes with 29% of the population comprised of adult barnacles (> 9 mm RC length), At the lower limit of the midtidal zone, where barnacles were interspersed among mussels (0.5-l m above MLLW), the population again becomes bimodal, with 28 % > 9 mm in RC length. Larger adults, > 18 mm RC length, comprise 18% of the total population. The settlement and recruitment of Pollicipes as a function of tidal exposure (March 1985) is given (Table XI).There is no difference in the settlement patterns (mean number of attached spat - barnacle- i), however, the recruitment patterns tend to show a greater survival of juveniles in the l-9 mm class at the lower midtidal level. The relationships between spat settlement and juvenile survival (recruitment) and the size of established aggregates (March 1985) are given (Table III). There is a positive relationship between the size of the aggregate and spat settlement. Recruitment and juvenile su~ivorship is also a function of aggregate size where the percent survival of juveniles is greater on the solitary barnacles than on the larger mixed barnacle-mussel aggregates. RECRUITMENT
EXPERIMENT
Excluding encrusting algae and diatoms, the initial colonizers of the denuded vertical rock surfaces were spat of the barnacle ~hthffrnal~s~~~ which first appeared during late January 1984. By May of the same year, no mussels or Pollicipes had established
D. L. HOFFMAN
90
SIZE
25
20.
15.
MID
% 101
5.
5
10
SILL
15
20
SETTLEMENT
AND RECRUITMENT
91
IN POLLICIPES
TABLE II Spat
settlement
of Policipes off La Jolla, (March 1985).
and recruitment
California,
as a function
of tidal
exposure
Position
n
X number of spat + SE adult barnacle _ ’
X number of recruits + SE adult barnacle - ’
High midtidal 2 m above MLLW Midtidal l-l.5 m above MLLW Low midtidal 0.5 m above MLLW
135
22.36 f 2.33
0.51 & 0.09
96
45.89 f 4.91
0.64 f 0.10
60
33.1 f 3.36
7.07 +_ 1.10
TABLE III Relationship
between
spat
Type of assemblage
settlement
n
and recruitment of juveniles (March1985). X number of Spat 2 SE adult barnacle -
’
and size of barnacle
2 number of juveniles + SE adult barnacle -
aggregation
y0 Survival from spat to juvenile
’
Solitary adults Very small aggregate (4-10. aggregate‘) Small aggregate (20-30. aggregate‘)
51 73
8.2 + 16.48 k
3.5 1.84
0.99 f 0.45 0.59 f 0.31
12.1 3.6
56
25.50 +
3.64
2.63 f 1.40
10.3
Mytilus-Pollicipes
52
3.95 f 1.51
3.1
105.90 & 12.951
mixed aggregate
themselves in these open areas. I was not able to return to these rocks until March 1985. At that time, a mixed band ofMyti1u.rcalijGmianus and Pollicipes had become established on the surfaces (Fig. 4). Destructive samples of this assemblage were compared to an assemblage at the same tidal level from the La Jolla seawall to determine differences in settlement and recruitment rates (Table IV). By this date, 17 months after initiating the experiment, adults > 15 mm RC length were found. 33 % of the adults > 10 mm had in excess of 200 spat attached to their peduncles. Recruitment rates were high and compared favorably with aggregates taken at the same tidal level on the seawall.
Fig. 3. Size-frequency distributions of population structures of Pollicipes at three different tidal levels on Children’s Pool seawall (March 1985). HIGH, 2 m above MLLW; MID, l-5 m above MLLW; LOW, 0.5 m above MLLW.
92
D. L. HOFFMAN
*1
93
SETTLEMENT AND RECRUITMENT IN POLLICIPES TABLE IV
Spat
settlement
Location
Recolonized rock La Jolla seawall
and
recruitment
n
37 52
of juveniles into recolonized (March 1985).
barnacle-mussel
assemblage
X number of spat + SE adult barnacle- ’
.iE number of recruits & SE
140.68 & 14.56 105.90 + 12.95
6.00 + 1.28 3.95 & 1.47
*adult bamacie - ’
DISCUSSION Pa~lic~es grow rapidly off La Jolla, at least in newly established aggregates. Spat
under Barnacle Rock grew at the mean rate of = 9 mm RC length in z 1 month after settlement. The barnacles invariably remained protected from desiccation on the inverted horizontal surface beneath the rock and received food from the surging water that had undercut the rock. Previously, I showed that under the artificial constraints of total submergence in fast-flowing aerated water in the Scripps intake seawater system Pollicipes could grow quite rapidly reaching a mean size of 4 mm in just 28 days (Hoffman, in press). However, these measurements included spat (O-l mm RC length) which lowered the mean size of the sample. Such rapid growth rates for pedunculate barnacles have been reported in other species. Macintyre (1966) reported that the opportunistic Lepas anatifera and Conchoderma virgata require from 17 and 50 days, respectively, to reach reproductive size in tropical waters. 17 days after a newly painted marker buoy was laid off the east coast of Australia, reproductive specimens of Lepas 23 mm capitular length were measured. Most measurements of Pollicipes indicate that the growth of the barnacle averages 1.2 mm * month- ’ (Paine, 1974), but these data were collected from barnacles growing in already well established aggregates. Page (1986) demonstrated that interspecific pressure exerted by the larger adults may inhibit the growth of smaller juveniles in such aggregations. Along the coastline of La Jolla, Pollicipes settles year-round on the peduncles of conspecifics with peak settlement beginning in the early spring (March-April). At this time, the larvae tend to settle in aggregative pattern at the proximal end of the peduncle just under the rostra1 and carinal margins of the capituium. This proximal end of the peduncle is a zone of growth producing new cuticle which may be attracting settling larvae (Darwin, 1851; Hoffman, 1984). Also this region of the animal is not in contact with adjacent barnacles and affords an exposed attachment surface. The density of
Fig. 4. Recruitment experiment. (A) Vertical seaward-facing rock with 0.75 x 1m area denuded (scraped) of all macroscopic organisms (October 1983). Note crack or fissure in rock (arrow). (B) Same rock surface on March 1985 colonized by ~ytil~ and PolZkzpes.(C) Close-up photo~aph of new P~~l~c~~es-~~i~l~s assemblages along fissure area of rock.
94
D. L. HOFFMAN
recently settled spat can be remarkable, > 300 * cm - ’ cm of peduncular surface. More accurate settlement rates could have been defined if the mean number of spat per unit area of stalk surface were determined. However, such determinations proved to be very difficult to make since the spat were patchily distributed on the peduncles. Usually, the spat were just proximal to the rostrum and carina. Also, the surface area of adult peduncles is not directly proportional to the RC length. Often, large adults with relatively large peduncular surface areas would house few or no spat. The reason for these variations is not known. Many of the larger and obviously older barnacles often have epiphytic algae attached to their peduncles which may impede larval settlement. Rarely, if ever, are young spat observed on any of the capitular plates. However, when adults are constantly immersed in running seawater (the Scripps seawater system), cyprid larvae do settle on the capitular plates and valves and grow into juveniles (Hoffman, in press). This indicates that the distribution of juveniles on adults may be due in part to their ability to withstand desiccation. During the months that these observations and measurements were taken, there was little evidence that Pollicipes cyprid larvae were establishing new aggregates on open hard substrates, excluding the underside of Barnacle Rock. The rocky surfaces adjacent to established aggregates were scrupulously examined with a magnifying glass on each monthly data collecting trip. On 2 September 1983, what appeared to be a newly established aggregate (2 x 6 cm) was observed along a rock fissure at the 0.5 m MLLW level. Small juveniles (the largest measuring 6 mm RC length) comprised this aggregate. However, 2 days later, the aggregate had been obliterated by beach sand, apparently smothering the barnacles. The recolonization of denuded vertical facing boulders by Pollicipes took in excess of 7 months which tends to run contrary to what occurred under Barnacle Rock. This difference may be explained by the orientation and exposure of the substrata. At Barnacle Rock, the settlement area was the horizontal undersurface of a rock, relatively protected from desiccation. The denuded rocks were seaward facing vertical surfaces, exposed to the drying rays of the sun at low tide, Settlement probably occurred at some time during the summer months. Inferred from the position of the barnacle aggregates (Fig. 4), initial settlement may have begun in a small crevice that ran along the face of the boulder. The survivors served as founders that attracted other barnacle settlers. Mortality during the fust 2-3 wk after settlement is relatively high in PoZIicipesspat. Connell (1961) suggested that mortality of ~e~ib~Zunu~ b~~~noi~esduring settlement periods was independent of settlement density and may be due to such physical factors as storms and periods of dry weather. Although I have no experimental evidence regarding the cause of this high mortality, there is observational evidence that it may be due in part to their position in the intertidal zone. During winter storms and also during hot dry periods of low tide exposure, mortality may be quite high. In addition, much sand and surf grass debris was usually embedded between or wrapped around the peduncles. These inclusions, in association with rows of minute cdcareous peduncular spines may have abrasive action on the spat and juveniles. Finally,
SE~LEME~
AND RECRUITMENT
IN
POLLICIP~~
95
numerous species of invertebrates within the aggregates may affect mortality. I observed on at least six occasions the nemertean Emplectonema gracile apparently foraging on small juveniles (1 mm RC length). The worms often were wrapped around small juveniles, many of which lacked capitula. Large numbers of polyclad flatworms, crabs, amphipods, and opisthobranch mollusks, all possible predators of young animals, also reside within the barnacle aggregates. Restriction in growth rates and survival of recent recruits of Pollici~es also is reportedly due to competition between the estab~shed adults and the recruits for food resources (Page, 1986). When large adults were expe~ment~ly removed from an aggregate, the smaller barnacles were able to increase rapidly in size. Page postulates that the large barnacles may interfere with the water flow that brings food to the smaller barnacles. In the mussel M’tilus edulis, Kantsky (1982) also reported that growth was suppressed in small mussels by increased density of large mussels. There appears to be a correlation between survival of recruits and the position of the recruits within the intertidal (Table II). The settlement rates of spat as a function of tidal position is consistent, indicating that the survival of the recruits may be independent of settlement density. However, juvenile survival also tends to be variable and dependent on clump size (Table III). The percent survival of juveniles is high on solitary barnacles which are encountered throughout their vertical distribution. Even though settlement is relatively sparse, recruitment is high. Whether or not these solitary barnacles serve as founders of new aggregates could not be determined during the course of these studies, however, Lewis (pers. comm.) indicates that such solitary adults may represent remnants of destroyed aggregates. Connell (1961, 1970) has demonstrated in acorn barnacles that predation plays an important role in recruit survival at their lower intertidal limit. In the lower levels of its dist~bution, Pollicipes is typically associated with mussels, either M. cu~~~~ianu~or M. edulis. Although the interaction between barnacles and mussels has been reported to be highly competitive for space, there may be positive value afforded by this relationship to the barnacle. In a homogeneous barnacle assemblage, there is little space between the peduncles for juveniles to attach to the primary substratum. However, in a mixed barnacle-mussel assemblage, the convex shells of the bivalves disrupt the space available to the larger adult barnacles affording room for the smaller juvenile recruits. When a section of barnacle-mussel assemblage is lifted off the substratum, large numbers of small Pollicipes (RC lengths < 6 mm) can be found attached directly to the substratum. Is it m~adaptive for Po~Zicipeslarvae to settle on the peduncles of conspeci~cs? These data indicate that barnacles with RC lengths > 9 mm are attached to the rocky substratum, whereas those below this size class tend to be attached to adults. In previous papers (Hoffman, 1981, 1984), I gave indirect evidence that the juveniles of Pollicipes may have limited mobilities by producing peduncular extensions at the distal end of the peduncle which seeks and attaches to the primary substratum. Within barnacle aggregates, many juveniles (RC lengths of I9 mm) may be found with these rhizoid-like processes extending downward from the adult peduncle (Fig. 5). The distal end of the
96
D. L. HOFFMAN
peduncle apparently also can give rise to new cuticle (ChatTee & Lewis, 1988). The circulatory pressure within the peduncle is reportedly one ofthe highest in the Crustacea, as high as 33 km. mm2 (Crenshaw, 1979; B. Burnett, pers. comm.). These high pedun-
Fig. 5. Juvenile Pollicipes(6 mm RC length) attached to peduncle of adult Pollicipes( 14 mm RC length). Note light-colored peduncular extension forming from distal end ofjuvenile peduncle. In living specimens, these extensions appear bright red due to thinness of cuticle and hemoglobin contained within.
cular pressures in association with cuticular growth zones might be used in association not only to extend the capitulum upward when feeding and during copulation between adults, but also to thrust the newly formed extension downward to find a new attachment site. These extensions also appear to carry ducts from the cement glands that adhere them to a new site on the primary substratum (pers. obs.). Therefore, preferential attachment of larvae on conspecifics may be highly adaptive to the surviving recruits,
SETTLEMENT
AND RECRUITMENT
IN POLLICIPES
91
for not only does it afford initial survival value for the fragile spat against desiccation, but also serves as an effective conduit that allows their eventual attachment to the primary substratum.
ACKNOWLEDGEMENTS
I thank W. A. Newman, P. K. Dayton, J. Barry, R. McConnaughey and B. Burnett for their help with this project. To C. A. Lewis and two anonymous reviewers, my thanks for their critical review of this paper. I also thank my wife Marcia and sons Noah and Tyler. This research was supported in part by a grant from the National Science Foundation, OCE-8 120943, and a faculty development grant from Bucknell University.
REFERENCES Barnes, H. & E. S. Reese, 1960. The behavior of the stalked intertidal barnacle Pollicipes polymerus J.B. Sowerby, with special reference to its ecology and distribution. J. Anim. Ecol., Vol. 29, pp. 169-185. Chaffee, J. & C.A. Lewis, 1988. Pendunculate barnacle stalk growth. J. Exp. Mar. Biol. Ecol., Vol. 124, pp. 145-162. Cimberg, R.L., 1981. Variability in brooding activity in the stalked barnacle, Pollicipespolymerus. Biol. Bull., (Woods Hole, Muss. ), Vol. 160, pp. 31-42. Connell, J. H., 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology, Vol. 42, pp. 710-723. Connell, J.H., 1970. The predator-prey system in the marine intertidal region. I. Balunus glandula and several species of Thaic. Ecol. Monogr., Vol. 40, pp. 49-78. Connell, J. H., 1985. The consequences ofvariation in initial settlement vs. post-settlement mortality in rocky intertidal communities. J. Exp. Mar. Biol. Ecol., Vol. 93, pp. 1 l-45. Crenshaw, D.G., 1979. Hydrostatic support of the pedunculate barnacles, Pollicipes polymerus. Comp. Biochem. Physiol., Vol. 62A, pp. 423-425. Darwin, C., 1851. A monograph on the class Cirripedia, with figures of all species. The Lepadidae; or pedunculate cirripedes. The Ray Society, London, 400 pp. Dayton, P. K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 35 l-389. Hand, C., J.D. Standing & J.C. Rutherford, 1973. San Francisco oil spill, effects on reproduction in intertidal invertebrates (Project No. 15080). U.S. Environmental Protection Agency, Washington, DC., 46 PP. Hilgard, G. H., 1960. A study of reproduction in the intertidal barnacle, Mitellapolymerus, in Monterey Bay, California. Biol. Bull. (Woods Hole, Muss.), Vol. 119, pp. 169-188. Hoffman, D.L., 1981. Foot-loose barnacles: implication of the retention of mobility into the postmetamorphic stages of the goose barnacle. Am. Zool., Vol. 21, p. 969 (abstract). Hoffman, D. L., 1984. Size-frequency distribution patterns ofthe juvenile stages ofthe pedunculate barnacle, Pollicipes polymerus Sowerby, 1833 (Cirripedia, Lepadomorpha). Crustaceana (Leiden), Vol. 46, pp. 295-299. Hoffman, D.L., in press. Settlement and growth of the pedunculate barnacle, Pollkzpespolymencs Sowerby, in an intake seawater system at the Scripps Institution of Oceanography, La Jolla, California. Pact? Sci. Kantsky, N., 1982. Growth and size structure in a Baltic Myrilus edulis population. Mar. Biol., Vol. 68, pp. 117-133. Lewis, C. A., 1975. Some observations on factors affecting embryonic and larval growth of Pollicipes polymerus (Cirripedia, Lepadomorpha) in vitro. Mar. Biol., Vol. 32, pp. 127-139. Lewis, C. A. & F.-S. Chia, 1981. Growth, fecundity and reproductive biology in the pedunculate cirripede,
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Pollicipes polymerus at San Juan Island, Washington. Can. J. Zool., Vol. 59, pp. 893-901. Macintyre, R. J., 1966. Rapid growth in pedunculate barnacles. Nature (London), Vol. 5062, pp. 637-638. Page, H.M., 1983. Effect of water temperature and food on energy allocation in the stalked barnacle, Pollicipespolymerus Sowerby. J. Exp. Mar. Biol. Ecol., Vol. 69, pp. 189-202. Page, H.M., 1986. Differences in population structure and growth rate of the stalked barnacle Pollicipes polymerus between a rocky headland and an offshore oil platform. Mar. Ecol. Prog. Ser., Vol. 29, pp. 157-164. Paine, R.T., 1966. Food web complexity and species diversity. Am. Nat., Vol. 100, pp. 65-75. Paine, R.T., 1974. Intertidal community structure. Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia (Berlin), Vol. 15, pp. 93-120. Ricketts, E. F. & J. Calvin, 1968. Between Pacific tides (revised by J. W. Hedgpeth). Stanford University Press, Stanford, California, 614 pp. Straughan, D., 1971. Breeding and larval settlement of certain intertidal invertebrates in the Santa Barbara Channel following pollution by oil. In, Biological and oceanographic survey of the Santa Barbara oil spill 1969-1970, Vol. I, edited by D. Straughan, Allan Hancock Foundation, University of Southern California, Los Angeles, pp. 223-244.