population regulation in the intertidal limpet patelloida alticostata (angas, 1865)
TRANSCRIPT
Oecologia (Berl.) 30, 9-22 (1977) Oecologia �9 by Springer-Verlag 1977
Population Regulation in the Intertidal Limpet Pa telloida alticosta ta (Angas, 1865)
Robert Black Department of Zoology, University of Western Australia, Nedlands, Western Australia 6009, Australia
Summary. Subpopulations of the limpet, Patelloida alticostata, converged slowly toward a density of about 75 per linear meter of vertical rocky shore two years after experimental alteration of densities of adult animals. The changes in number of limpets in subpopulations occurred because large limpets suffered considerable mortality, while recruits experienced almost none. Neither migration, cannibalism, selection of settlement site by the limpets, nor predation by a whelk, acted in a density-dependent manner.
Growth rates were density-dependent, and juveniles and recruits reached a much larger size in the absence than in the presence of adult limpets. Increasing the density of adult limpets did not increase the extent of grazing areas and subpopulations of different size compositions utilized similar graz- ing areas. Food may have been in short supply.
These limpets have a great deal of population inertia, accommodating sporadic good recruitment by compensations in growth rates.
Introduction
This paper reports observations and experiments with an intertidal acmaeid limpet, Patelloida alticostata (Angas, 1865). The basic questions were: does this limpet show the same rapid adjustment stability or population regulation that communities of limpets have shown elsewhere (Stimson and Black, 1975) and, if so, what are the mechanisms? The central approach to these questions was examination of population characteristics after experimental alteration of the density of adult limpets in replicated subpopulations.
Limpets have been popular subjects for field studies and yet, deliberate alteration of densities with the purpose of analysing population responses are few (Frank, 1965; Breen, 1971, 1972; Haven, 1973; Lewis and Bowman, 1975; Stimson and Black, 1975). Three general mechanisms which could act to regulate population density have been either demonstrated to occur, or appear to be reasonable hypotheses needing testing. First, density dependent migration occurs
10 R. Black
in Acmaea digitalis (Frank, 1965; Breen, 1972), but rigorous evidence seems lacking for other species. Second, cannibalism of newly settled recruits by larger limpets has been proposed by Branch (1971), Stimson and Black (1975), and Lewis and Bowman (1975). None of these show direct evidence of this phenome- non. Since the susceptible recruits are so small, direct observations are difficult and removal of adult limpets while preventing cannibalism probably also alters the amount and kind of algae on the surfaces. Third, selection of suitable substratum may determine the abundance and location of recruitment. Different species show avoidance of areas of macro algae (Southward, 1955), but high abundance in damp locations (Lewis and Bowman, 1975), on wave beaten
�9 shores (Branch, 1975 a), and where there are already adults (Black, 1976; Branch, 1975a).
To regulate populations, the outcome of these three mechanisms should be density dependent movement, perhaps even leading to mortality of adults, increased mortality of recruits at high adult densities, and reduced recruitment at high adult densities. Any of these or other proposed mechanisms for population regulation must act to decrease high population and increase low population.
P. alticostata is widely distributed in southern Australia, occurring from southern Queensland to the Murchison River, Western Australia (Dakin et al., 1969; Cotton, 1959). On Rottnest Island, Western Australia, it is abundant in two sorts of habitat (Hodgkin et al., 1959). On the fiat limestone platforms which become exposed during low tide, these limpets occur at very high densities (Hodgkin, 1959, 1960). Their shells, and the rock, are encrusted with coralline algae. Limpets from this habitat were not studied. The second habitat is the base of the vertical limestone rock which forms the shoreward boundary of the platforms. There, the limpets live in a band 30 to 60 cm high, are at lower densities than on the platform, and reach a larger size. In many cases these limpets are isolated from their fellows on the platform by sand, rough textured rock, or depressions in the platform. In all study areas on the vertical rock, coralline algae are rare or entirely absent. The limpets graze on micro-algae, macroscopic turf-like forms, and, perhaps, Ulva. In Victoria, Australia, P. alti- costata consumes mostly calcareous algae (Parry, 1975, personal communication; Synnot and Wescott, 1976).
Other published references to biology and ecology of P. alticostata are few. Anderson (1965) described the eggs and early life of the free-swimming trocho- phores which, at 20~ become permanently crawling larvae six days after fertilization. Bennett and Pope (1953, 1960) describe P. alticostata distribution in south-eastern Australia and Tasmania, where it is common, but not a domi- nant species. More recent descriptions of zonation of communities containing this limpet are by May et al. (1970) and Synnot and Wescott (1976).
Methods
Observations on Natural Populations of Limpets
In order to determine whether the abundance or size distribution of limpets affected recruitment to populations of P. alticostata, limpets were counted along the vertical limestone shores of ten
Population Regulation in a Limpet 11
beaches at Rottnest Island. At r andom intervals, 25 x 25 cm quadrats were placed without reference to the nature of the rock or the limpets. The limpets were assigned to three size- and, presumably, age-classes which did not overlap at that time of year. Adult limpets were greater than 25 m m long, had greater shell height than other size classes, and had eroded shells or growths of epiphytic algae on them. Juveniles were 15--25 m m long, had uneroded shells, and were bare of epiphytic algae, except for a slick of unicellular green algae. Recruits were 5 15 m m long and were conspicuous because the black and white pattern of their ribbed shells contrasted with the rock.
To estimate movements and growth rates of limpets in low density conditions, the location of each adult and juvenile limpet at the Strickland Bay (West) site were mapped on four occasions; 24 October, 15 November and 30 December 1974, and 23 November 1975. Their lengths were measured on 24 October 1974 and 23 November 1975.
In locations where the density of adult limpets was low, the grazing area was often a conspicuous patch of bare rock surrounded by an algae turf. To determine how much area individual uncrowded limpets require, the length of the limpet and the length and breadth of the grazed areas containing a single limpet were measured. The area of an ellipse with those axes provided an estimate of the area grazed by each limpet. Al though this method is less accurate than Stimson's (1970), it is much faster and allows greater sample sizes.
To estimate the rate and seasonality of mortality of P. alticostata, and the contribution of predation by Dicathais aegrota (Reeve, 1846) to this mortality, all the recently dead limpet shells within 2 m of the base of a 70 m section of the vertical shore at Radar Reef were collected. Twenty collections were made between l January 1975 and 20 January 1976.
Manipulation of Limpet Densities
The experimental test for population regulation, explained by Murdoch (1970), and previousIy used by Stimson and Black (1975) requires that subpopulat ions which have been manipulated previously to different densities converge to a single density. On 18 October 1974 such an experiment was initiated on 20 m of vertical limestone shore using four density treatments: adult density doubled, density unaltered, adult density decreased by half, and all adult limpets removed. Treat- ments were assigned at random within matched groups of sections of the shore. The experimental zones were contiguous along the shore. Their boundaries were defined by paint marks at the upper limit of the distribution of the limpets. No at tempt was made to prevent limpets from moving from one zone to the next, al though some of the angles, corners, and discontinuities of the shore were probably barriers to lateral migration. The base of the shore was sand-covered, so there were few limpets living on the horizontal rock and migration to and from the experimental zones was negligible.
This particular portion of the shore was chosen because there were large numbers of recruits, juveniles, and adult limpets. Of particularly interest was the evaluation of the effects on these size-, age-classes by the disturbance of adult limpet densities.
In order to follow the survival, growth, and movements of juvenile limpets, each individual was tagged on 30 December 1974, and at the same time, all the adults were counted and each juvenile and recruit measured. The procedure was repeated on 23 November 1975 and 28 October 1976 for all limpets.
As another measure of limpet growth, two or usually three colour transparency slides were taken of 300 cm 2 areas in each experimental zone on four occasions between November 1974 and 1975. These areas were chosen to include as many recruits and juveniles as possible, but were at slightly different locations each time. The max imum length of the projected image of each limpet was measured, and the actual limpet size obtained by correcting for the magnification of the projection.
To determine whether a predator could cause density-dependent mortality among the experimen- tal limpets, on 22 occasions between 15 November 1974 and 19 January 1975, the number of D. aegrota actually on the vertical portion of each experimental zone, and the six other zones intermingled with the experimental ones were counted. Each snail was examined to detect if it were feeding.
12 R. Black
Results
Density Differences among Sites
The density of P. alticostata was patchy in space (between sites) and in time (within sites) during the two years of observation (Table 1). Under natural conditions these ten sites on Rottnest Island had, on the average, from 5.0 to 0.3 adults, f rom 5.8 to 0.0 juveniles, and from 7.8 to 0.0 recruits per 625 cm z. The patterns of differences in density of limpets have been analyzed in several ways. First, a two-way analysis of Variance with no replication of the mean total density of limpets in the eight sites with complete data for three sets of observations showed significant heterogeneity among sites (F = 24.04; 7,14 df; P < 0.005) and among years ( F = 8.53 ; 2,14 df; P < 0.005). The density of limpets decreased significantly each year from 7 to 5 to 4 limpets per 625 cm 2 (Student- Newman-Keuls test). Adults and recruits were significantly less abundant and juveniles more abundant in 1975 than in 1974 (matched-pairs signed-rank tests, two-tailed, 0.02 > P > 0.01, P = 0.05, and 0.05 > P > 0.02 respectively). Similarly, only recruits were less abundant in 1976 than in 1975 while adults and juveniles were no different (P = 0.01, P ~> 0.05, P >> 0.05 respectively). The large recruitment of small limpets in 1974 seemed reflected in the increased number of juveniles
�9 in 1975 which suggested that recruits grew into the juvenile size class in 1 year.
Evidence for Population Regulation
The raw census data from the 13 experimental zones in which the density of adult limpets was altered indicated that the adults suffered considerable mortality. Of 368 adults alive in December 1974, only 236 remained in November 1975. Only two zones had greater numbers (a total of 3 limpets) in 1975 than in 1974. The juveniles fared better with 152 remaining out of an original 172. Only three zones had increased numbers of juveniles (8, 5, and 4). This could have resulted from migration or confusion of size classes. In contrast, the recruits were more abundant in November 1975 than in the previous year (cf. 637, 580). This means a failed to detect all the recruits in the December 1974 census, that settlement of additional recruits continued after December 1974, or both. This same result occurred in the area where the locations of limpets were mapped. There were 141 recruits in 1974 and 185 in 1975. Survival of recruits must be good.
Did these limpets show evidence of population regulation? Since the experi- mental zones were of unequal size, census data were converted to numbers per 1 linear meter of shoreline (Table 2). If the P. alticosta subpopulations in the experimental zones are regulated, densities should decreases following an increase in density, and increase following a decrease in density. These changes should be judged relative to the unaltered control treatments. In fact, the greatly decreased and increased density treatments converged in 1976 to an average of about 88 limpets per linear meter, while the control and decreased treatments converged to an average of about 65 limpets (Table 2).
Tab
le 1
. M
ean
num
bers
(_
+ st
anda
rd
erro
r)
of P
a)el
loid
a al
tico
stat
a in
62
5 cm
2 qu
adra
ts.
A=
adu
lt,
J=ju
veni
le,
R=
recr
uit.
L
ocat
ions
ar
e on
th
e so
uth
o si
de o
f th
e is
land
and
lis
ted
in o
rder
fro
m w
est
to e
ast
Loc
atio
n 19
74
1975
19
76
Sam
ple
A
J R
S
ampl
e A
J
R
Sam
ple
A
J R
si
ze
size
si
ze
=~
Cap
e V
lam
ingh
12
5.
00
0.25
0.
00
28
2.07
0.
10
0.00
52
1.
54
0.14
0.
00
(0.9
4)
(0.1
8)
(0.4
9)
(0.0
6)
(0.2
3)
(0.0
7)
Fis
h H
ook
Bay
20
0.
60
0.00
0.
00
50
0.40
0.
18
0.02
53
0.
32
0.04
0.
00
(0.2
2)
(0.0
9)
(0.0
8)
(0.2
2)
(0.0
7)
(0.0
3)
Rad
ar R
eef
13
4.38
0.
23
0.23
50
3.
76
0.10
0.
22
85
2.88
0.
53
0.07
(0
.56)
(0
.17)
(0
.29)
(0
.05)
(0
.07)
(0
.17)
(0
.66)
(0
.34)
S
tric
klan
d B
ay (
Wes
t)
Map
ped
graz
ing
area
27
-
- 7.
85 a
18
0.
83
5.83
1.
11
12
6.25
1.
17
0.00
(1
.93)
(0
.17)
(0
.72)
(0
.21)
(0
.73)
(0
.37)
A
mon
gst
grou
ped
11
3.55
2.
09
7.82
15
1.
33
5.53
0.
73
7 4.
43
0.71
ad
ults
(0
.39)
(0
.34)
(1
.18)
(0
.39)
(0
.87)
(0
.25)
(0
.30)
(0
.18)
W
ithi
n de
nsit
y 28
5.
68
2.68
6.
39
37
4.43
8.
65
0.89
23
8.
70
3.00
0.
35
man
ipul
atio
n zo
nes
(0.8
5)
(0.2
9)
(0.7
8)
(0.4
6)
(0.5
9)
(0.1
8)
(0.8
1)
(0.4
5)
(0.1
6)
Eas
t of
zon
es
28
7.04
1.
08
4.39
19
2.
95
3.84
0.
05
25
4.63
1.
12
0.16
(0
.26)
(0
.28)
(0
.80)
(0
.41)
(0
.75)
(0
.05)
(0
.69)
(0
.35)
(0
.08)
S
tric
klan
d B
ay (
east
) 56
4.
14
0.45
0.
48
71
2.33
0.
97
0.59
45
2.
00
1.31
0.
02
(0.2
2)
(0.1
2)
(0.1
2)
(0.2
2)
(0.1
5)
(0.1
0)
(0.1
9)
(0.2
1)
(0.0
2)
Gre
en I
slan
d 14
0.
29
0.37
0.
64
35
0.31
1.
00
0.23
37
0.
43
0.43
0.
00
(0.1
3)
(0.2
3)
(0.2
2)
(0.1
3)
(0.1
7)
(0.0
8)
(0.1
0)
(0.l
l)
Par
ker
Poi
nt
20
- 0.
25
60
1.95
0.
43
0.15
49
1.
55
0.27
0.
00
(0.1
2)
(0.2
0)
(0.0
9)
(0.0
5)
(0.2
0)
(0.0
8)
- =
data
not
col
lect
ed
Thi
s fi
gure
is
not
calc
ulat
ed f
rom
qua
drat
co
unts
, bu
t ra
ther
by
extr
apol
atio
n to
num
bers
of
rec
ruit
s w
ithi
n m
easu
red
graz
ing
area
s ha
d th
ose
area
s be
en 6
25 c
m 2
14 R. Black
Table 2. Number of limpets per 100 cm in zones on the lower portion of vertical coastal limestone at Strickland Bay, Rottnest Island. Corresponding rows in each treatment are matched zones. The mean number of adult limpets in the 13 experimental zones was 31 limpets per 100 cm. Juveniles and recruits were not altered in any treatments
Adult Width December 1974 limpet of treatment Zone Adults Juve- Re-
cm niles cruits
November 1975 October 1976
Adults Juve- Re- Re- All limpets Re- niles cruits cruits except 1976 cruits 1974 1974 1975 recruits 1976
Increased 106 57 13 55 90 60 17 71
102 39 8 44 Unaltered 138 37 9 24
84 50 19 68 73 29 16 59
114 22 15 22 Decreased 136 17 6 17
107 16 15 48 108 13 14 17
Greatly 105 2 20 57 Decreased 125 4 10 63
84 14 5 29 Unaltered 128" 11 10 26 but not 100 25 7 21 matched 45* with ex- 125 21 5 12 perimental 94 27 4 10 zones 104 18 7 7
34 12 58 12 92 3 31 17 67 3 97 1 16 9 47 5 69 0 26 14 20 6 50 4 35 11 74 9 103 1 25 12 63 4 60 3 15 18 26 2 49 3 12 10 25 2 45 2 11 9 66 6 87 2 15 8 28 1 50 2 3 14 69 23 110 7 1 4 73 4 79 2
10 4 42 6 68 0 3 14 27 2 51 0
25 28 11 2 56 2 27 9 27 0 60 0 14 14 17 1 41 1 15 10 14 6 28 2 7 5 11 5 12 3
Before manipulation October 1974 mean (standard error) n= 17 29.4 10.6 29.8 Does not include* (1.84) (1.12) (4.46)
J u d g e d by the test sugges t ed by M a c A r t h u r a n d C o n n e l l (1966) a n d used
by S t i m s o n a n d B l a c k (1975), t hese l i m p e t s u b p o p u l a t i o n s s h o w e d e v i d e n c e
o f a s low r e t u r n t o w a r d an ' e q u i l i b r i u m ' p o p u l a t i o n size ( T a b l e 3). In this test, the c h a n g e in dens i ty b e t w e e n censuses (I1) is p l o t t e d aga in s t the in i t ia l
dens i ty (J0 . T h e va lue o f J ( w h e n Y = 0 ind ica t e s the ' e q u i l i b r i u m ' dens i ty
A s lope o f - 1 . 0 w o u l d i nd i ca t e ' p e r f e c t r e g u l a t i o n ' . I f the s u b p o p u l a t i o n s c o n t i n u e to c h a n g e in dens i ty as t hey h a v e d o n e b e t w e e n 1974 a n d 1976, c o n v e r -
�9 gence to the ' e q u i l i b r i u m ' dens i ty o f 69 wil l t ake severa l a d d i t i o n a l 2 -year pe r iods .
Th i s k i n d o f ana lys i s was a p p l i e d to the s ize-classes o f l impe t s , too , to
test h o w these c o m p o n e n t s o f the p o p u l a t i o n r e a c t e d to e a c h o ther . B e t w e e n
1974 a n d 1975, the c h a n g e in dens i ty o f "adults on rec ru i t s was m o s t c lose ly r e l a t ed to the in i t ia l dens i ty o f adul t s , wh i l e j u v e n i l e s c h a n g e d a c c o r d i n g to the f t o w n in i t ia l dens i ty ( T a b l e 3). O t h e r in i t ia l dens i t ies , c o m b i n i n g d i f f e ren t
c o m p o n e n t s o f t he l i m p e t p o p u l a t i o n , p r o d u c e d r eg res s ions w h i c h e x p l a i n e d less o f the va r i ab i l i t y in c h a n g e s o f n u m b e r s .
Population Regulation in a Limpet 15
Table 3. Comparisons of changes in density of limpets (number per 1 m of shore) between censuses in 1974, 1975 and 1976 (10,and initial density in 1974 (X), for the 13 experimental zones. Only regressions with slopes significantly different from zero are listed
Comparison Regression P, /3=0 r 2 X when Y=0
X, Y for total limpets 1974 to 1975 Y=25.8-0.29 X <0.01 0.46 89 1974 to 1976 Y=38.6-0.56 X <0.01 0.57 69 1975 to 1976 Y= 17.0-0.28 X <0.05 0.27 6I
1974 to 1975
X= adult limpets Y=adult limpets Y= 3.1-0.46 X <0.001 0.83 7 Y=recruit limpets Y= 13.3-0.25 X <0.01 0.55 53
X, Y juveniles Y= 4.7-0.15 X <0.02 0.32 9
X - adults +juveniles Y=adult limpets Y= 6.7-0.41 X <0.001 0.73 16 Y= recruit limpets Y= 15.1 - 0.21 X < 0.01 0.48 72
X - total limpets Y=adult limpets Y= 8.0-0.21 X <0.01 0.55 38
The densities of adults, juveniles and recruits decreased in l l , 8, and 2 respectively, of the 13 experimental zones between 1974 and 1975. The percentage change in densities (Y) was related to initial densities (X) only for recruits' densities compared with adult densities (Y=40.54-0.75 X; n=13; r2=0.41; P,/3=0 < 0.02). This was because recruits increased in density most where adult densities were low (Table 2). Mortality rate of adults or juveniles does not increase with an increase in adult densities.
Migration
Under conditions in which density of limpets was unaltered, on a day to day basis, adult limpets return to a home scar after grazing during high tide. Sixty- seven individually identified limpets were in identical locations with identical orientation within their scars on four consecutive days at low tide. Twenty-three of these failed to move during the early part of low tide on three consecutive days, 26 moved on 1 day, 14 on 2 days, and 4 on all 3 days. Of course, all limpets may have moved later during the high tide, after observation, but these limpets show great fidelity to their home scars.
Over periods of weeks and months, mapped limpets did not always appear to be in the same location. This could be due to actual movements by the limpets. Displacements which were greater than 5 cm (i.e. greater than a measure- ment error) increased with time in a sample of 34 limpets present during 1974 and 1975 (Table 4). The overall displacements between 24 October 1974 and 23 November 1975 did not vary with the size of limpet, or with the growth of the limpets; the final locations of the limpets had no fewer limpets within
16
Table 4. Numbers and movements of P. alticostata in the mapped area
R. Black
24 Oct. 15Nov. 30Dec. 23Nov. 28 Oct. 1974 1974 1974 1975 1976
48 a 58 53 b 42 169
54 72 84} 185} 57 83
12 13
Number of adult limpets 1974 Recruits
in grazing areas outside grazing areas
1975 Recruits 1976 Recruits
Mean distance cm 3.6 +0.4 4.1 -+0.8 8.8 + 1.2 (-+ standard error) displaced from previous time by same 34 limpets
Range 0, 9 0,25 1, 25
Displacements > 5 cm 5 6 19
Mapped under poor conditions; some limpets missed b Sum of grazed areas is 0.88 m 2. In 1975 the 227 limpets had contiguous grazing areas estimated at 2.76 m 2
a circle of 15 cm radius than the original location. The stimulus that limpets to move was not detected.
Under the experimental conditions of altered densities of adult limpets, it was difficult to detect accurately lateral movement of individual adult limpets from zone to zone, because they were not individually marked. However, de- creased density zones did not increase in numbers corresponding to the decrease in numbers occurring in the adjacent high density zones.
Records of locations of tagged juveniles showed three juveniles had moved from increased and unaltered density zones and two from decreased density zones, while 21 and 14 remained in place. Migration of juveniles was neither extensive nor increased by high densities of adults.
As an estimate of vertical movements of limpets on 27 October 1974, and 25 January and 7 December 1975, the vertical extent of the grazing area of three places in each of the 13 experimental zones was measured and their average value to the nearest centimeter calculated. This value decreased between October and January in all cases except two, both in the treatments with in- creased density of adult limpets, but both with a value of only 1 cm. However, the decrease in height grazed in the six zones with adults removed was signifi- cantly greater than in the remaining seven zones (Mann-Whitney U test, P = 0.004). By December 1975, the changes from the October values were still all negative, save one, unchanged, of the unaltered zones. There was no signifi- cant difference in the magnitude of the change as previously (Mann-Whitney U test, P = 0.365). These results support two points. First, increasing the density of adult limpets did not appreciably increase the vertical extent of the grazing areas, but decreasing densities decreased grazing area. Second, the subpopula- tions made up of radically different densities of different size, age-classes (Ta- ble 2) came to utilize the same grazing area.
Population Regulation in a Limpet 17
Recruitment
Among the sites, the density of adult limpets was rather different. The data provided a test of whether recruitment varied with the abundance of older limpets on a between-site scale. Spearman rank correlations between the average number of recruits and the sum of adult and juvenile limpets are positive, but not significant in 1974 and 1975. The correlation is positive and significant in 1976 when recruitment was very low (rs=0.621, n = 10, P<0.05) . Therefore, recruitment to different sites does not tend to make densities uniform among sites, but may help to maintain density differences between sites.
Within the site chosen for the density manipulation experiment, the original censuses of 17 zones showed that the number of recruits per linear meter of shore in each zone (Y) increased as the number of adults plus juveniles (X) ( Y = - 2 5 + 1 . 3 8 X; n = 1 7 ; ra=0.59; /3=0, P<0.01). In the next year, recruit- ment was very much lower and the number of recruits per 1 m (Y) was unrelated to number of adults and juveniles per 1 m (X) ( Y = - 0 . 0 7 + 0 . 0 8 X ; n = 1 9 ; r2=0.15; / /=0, P>0.05) . Among the limpets whose positions were mapped, recruits were in grazed areas at mean densities of about 8 per 625 cm 2 compared with 2 in the adjacent ungrazed areas (Table 1, 1974).
In the experimental zones, the distribution of the 'ext ra ' recruits by treat- ments was not uniform. There were six additional recruits in zones where adults were increased, 12 where adults were unaltered, 39 where adults were decreased, and 38 where adults were greatly decreased. After alterations of numbers of adults, settlement in or movement to zones of high density was poor.
Agents of Mortality
What killed limpets? The predator D. aegrota frequented the zones where density of limpets was altered. The occurrences of this predator were not more frequent in zones where limpet were most abundant ( r = - 0 . 2 4 , n=17, P>>0.05) and so showed no numerical response to prey density. Howeverl P. alticostata made up 23% of the number of prey eaten by Dicathais (Table 5).
At Radar Reef, where shells of dead P. alticostata were easily collected, 106 of 299 recently dead shells were drilled by Dicathais. Significantly more
Table 5. Prey of 474 Dieathais aegrota examined on 22 occasions at the experimental zone, 15 November 1974 to 19 January 1976
Prey species Number of observations
Nodilittorina rugosa 2 Melaraphe unifasciata 2 Siphonaria baconi 1 Siphonaria luzoniea 17 Notoacmea onychitis 2 P. altieostata 8 Chiton 3
Total: 3 5
18 R. Black
shells were drilled during April to November (42 of 79) than during the rest of the year (64 of 220) (Z2= 14.73). Mortality of P. alticostata ad Radar Reef during summer may have been caused by heat and desiccation, as recently vacated home scars appeared during a hot period in January 1975. Thirteen of 18 vacated scars were in the sun at 1300 h, while only 20 of 65 m of the rock was sunlit at midday (7~z=12.44). Although the vacated scars belonged to adult limpets, it is not known if juveniles and recruits were similarly affected, due to their rarity at Radar Reef (Table 1).
Density and Growth Rates
The analysis of the growth of recruits and juveniles in the experimental zones also provides evidence to support the idea that the recruits were in their first year of life and juveniles in their second year, so that the adult size-class was made up of animals older than 2 years.
Table 6 shows that in November 1974 the recruits in the four adult density treatments were, on the average, close to 7 mm long. By the next year their average size was greatest where adult limpets were absent or reduced, and smaller where adult densities were normal or increased. The juveniles averaged about 15 mm long in November 1974, a size similar to the recruits after 1 year's growth. The adult density treatment affected their final size in November 1975, following the same pattern as for the recruits. Analysis of variance and Student-Newman-Keuls' tests showed that all pair-wise treatment comparisons were significantly different, except for the juveniles in both natural and increased density treatments, and the recruits in reduced and increased treatments. Both recruits and juveniles reached a much larger size in the absence of adult limpets.
On a zone by zone basis, the comparison of the mean increase in length of juveniles or recruits (Y) with the average density of limpets (X) in each zone showed that the growth increment decreased as density of adults and juveniles increased (juveniles Y=5.41-0.057X; n=17; r2=0.29; P,/~=0, <0.05; recruits u X; n=17, r2=0.47; P, fl=0, <0.01).
Growth rates of individually identified limpets were available from the tagged juveniles in the density manipulation zones, and from the mapped limpets. Increase in length (Y), compared with initial length (X in ram), gave Y= 18.5-0.53X(n=38, r~=0.56, P, /~=0<0.001) for mapped limpets, and Y= 10.0-0.3 X (n = 49, r 2 = 0 .09 ; P , fl = 0 < 0.05) for limpets in the zones. Juveniles in the mapped area grew about three times more than equivalent sized limpets in the zones (5.9 mm compared with 2.0 mm for limpets 24 mm long, P<0.001 by analysis of covariance). The recruits in the mapped area reached a mean size of 21.5 mm, significantly greater than the 15.9 mm of the recruits in the zones (t = 20.74). The presence of large numbers of adult limpets reduced the growth rate of smaller limpets.
For isolated individuals, the larger the limpet, the greater the space used for grazing activities (Table 7). The average adult-size limpet grazed in about 130 cm 2. Because individual grazing areas were absent from areas of high limpet density, grazing areas must overlap. Limpets at greater densities did not grow as fast as those at lower densities: food may have been in short supply.
Population Regulation in a Limpet 19
Table 6. Mean lengths (ram) _+ Standard error of the mean of juvenile and recruit Patelloida alticostata measured from colour slides taken of limpets in the zones of manipulated adult limpet density. The sample size is in paranthesis
Treatment Data
22Nov. 1974 26 Jan. 1975 28 May 1975 24Nov. 1975
Recruits Adult density
Increased 6.9-+0.20 8.7-+0.16 11.6-+0.26 15.0_+0.31 (50) (68) (44) (44)
Natural 7.3_+0.10 9.2-+0.15 12.2_+0.22 14.4_+0.36 (47) (72) (58) (49)
Reduced 7.5 _+ 0.30 9.2 _+ 0.20 13.7 _+ 0.40 16.2 + 0.29 (26) (51) (41) (41)
Absent 7.2 _+ 0.10 9.6 _+ 0.22 14.4_+ 0.34 17.7 _+ 0.27 (45) (55) (57) (72)
Juveniles
Increased 14.9 _+0.70 15.5 _+0.85 16.5 _+ 0.82 19.7 _+0.46 (12) (13) (14) (27)
Natural 15.4_+0.50 17.2_+0.40 17.2_+0.54 18.3_+0.63 (19) (24) (20) (18)
Reduced 16.1 _+0.70 18.7_+0.48 19.7_+ 1.13 21.7+_0.48 (9) (19) (17) (1 I)
Absent 14.5-+0.80 17.5_+0.85 23.6-+0.95 25.5_+ 1.95 (10) (13) (8) (3)
Table 7. Grazing areas of isolated Patelloida alticostata, Patellenax laticostata, and Lottia gigantea. Regressions are square root of grazing area in em 2 (10 on length of limpet in mm (i"). All slopes are significantly different from zero at P < 0.001
Species and Sample Regression r z Adj Y Adj Y Grazing location size for for area cm 2
X=45 mm X=31 mm for X=31 mm
P. alticostata
Mapped area 1974 27 Y : -2 .17+0 .45 X 0.73 18.23 Parker Point 1975 88 Y= - 1.56+0.42 X 0.44 17.48 Nacy Cove 1975 32 Y= 0.03+0.35 X 0.57 15.79
P. laticostata
Radar Reef 1975 59 Y= 4.24+0.21 X 0.37 13.59
L. gigantea
California (Stimson, 1970) 23 Y : 11.20+0.45 X 0.44 31.71
11.83 140 11.42 130 10.78 116
20 R. Black
Using a pooled equation relating grazing area used by isolated limpets to limpet length (Table 7), the amount of area that limpets in each experimental zone would require if they were all isolated was calculated. Comparing this area to the area actually utilized in 1975, calculated from the width of each zone plus the average height, showed that all but one zone had a smaller area grazed than the limpets might use if they were not crowded together. The magnitude of this area deficit did not differ between the six zones with decreased adult densities and the seven zones left unaltered or with increased adults (Mann-Whitney test, P = 0.314).
Discussion
The observations and experiments on P. ahicostata that deal with the three general mechanisms suggested for changes in numbers in limpet populations are as follows:
a) Density-dependent migration by adult or juvenile limpets does not occur. Adult limpets normally return after grazing excursions to scars on the rock to which their shells fit. Some limpets which were moved, shifted locations before they took up permanent positions. There was no indication that limpets assumed positions higher or lower in the intertidal zone, or expanded the vertical extent of their grazing activities. Some juvenile limpets did move to new posi- tions, too, but observations, although few, do not suggest that such movements are density-dependent. In the context of the experiment, migration fails to explain density-dependent changes in number of animals.
b) There is no direct evidence of cannibalism of young limpets by older ones. Rather, the indirect evidence suggests such a process may not be very important. When there was an abundant recruitment, the density of young limpets varied directly with the density of older limpets when areas of about 1 linear meter of shore were considered. On an even smaller spatial scale, young limpets were more abundant inside than outside grazing areas of adults. In both cases, subsequent survival of these recruits ( > 5 mm long) was excellent. No recruits less than 2 mm long were observed, and the possibility remains that cannibalism does occur before limpets reach 5 ram. However, these patterns of positive association between adults and young mean that cannibalism does not act in the required density-dependent manner. The only evidence of detrimental interactions of larger on smaller limpets, is that more additional recruits appeared in zones with decreased densities of adults than in zones where adults were unaltered or increased. The small number of limpets involved in this density-dependent feature was overwhelmed by the initial density of recruits, which were most abundant where adults were.
c) Selection of suitable substratum as a mechanism by which recruitment could increase numbers where older limpets are scarce and not augment numbers where limpets are abundant, does not occur in the P. alticostata of this study. The suitable substratum for these limpets, judged by where they occur in abun- dance for within-site conditions, is where adult limpets graze the surface. This
Population Regulation in a Limpet 21
association between older limpets and new recruits is also positive between sites. Good places for adults are good places for recruits which survive well and grow in this close accociation.
Since migration and recruitment do not act strongly in changing numbers in a density-dependent way, mortality may. The general trend over three years has been for numbers to decrease wherever the 1974 year class was small (Ta- ble 1). The only apparent agents of mortality observed were extreme heat, and desiccation, of which no more will be said, but which are discussed by Hodgkin (1960), and the predator Dicathais. If Dicathais ate P. alticostata at the rate of 8 in 22 days (Table 5), in the 331 days between the December 1974 and November 1975 censuses, they could consume 120 limpets. This matches reason- ably well with the 132 adult and 20juvenile limpets which disappeared during that time. It is unlikely that Dicathais took all those animals; at Radar Reef Dicathais drilled only about 35% of the total number of recently-dead limpets. In addition, Dicathais failed to occur in higher numbers in zones where adult limpets were most abundant, and it is, therefore, improbable that mortality by predation could have been density-dependent in this experiment.
The analysis of changes in limpet densities and the comparison with initial densities, although providing evidence of convergence and self-regulation, indi- cated a rather sl0w return towards an 'equilibrium' density (Table 3, no slopes about -1.0). These P. ahicostata populations show a great deal more inertia (c.f. Murdoch, 1970) than any of the other species in which density manipulation has been used to test for regulation (Stimson and Black, 1975). The major difference is that this limpet is apparently a long-lived animal in which abundant recruitment is sporadic. If animals grew each year according to the rates mea- sured in 1975, assuming they reached a length of 20 mm in 2 years (Table 6), it would take six additional years of growth at the rate achieved in the mapped area to reach 35 ram, which is about the maximum length. At the growth rate achieved in the experimental zones, where density of limpets was high, 20 mm limpets would take seven additional years to reach just over 29 mm, which is about the asymptotic size for that growth rate. Accurate age estimates of this limpet require additional detailed observations.
These limpet populations accommodated the sporadic good recruitment by compensations in growth rates. Growth rates of all size-classes decreased with density. Therefore, P. ahicostata displayed population regulation similar to that reported for Nerita atramentosa by Underwood (1976). Although the relation between density of limpets and mean size is negative for P. alticostata (Hodgkin, 1960), as for Cepaea nemoralis and Acmaea spp. (Haven, 1973), the mechanism explaining this phenomen is most probably competition for food, as in the case of.Nerity and Acmaea and not the chemical or behavioral interactions proposed for Cepaea by Williamson et al. (1976).
Acknowledgements. This study was financed by the Department of Zoology, University of Western Australia, and during its later stages by A.R.G.C. grant D1-75/15097. I thank D. Bray, R. Irving-Bell, B. Miller, and J. Turner who assisted in the field, and I. Abbott, P. Chalmer, and E.P. Hodgkin, who discussed the work. The Biological Research Station, Rottnest Island, provided accomodation.
22 R. Black
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Received February 12, 1977