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Population dynamics of the estuarine isopod Sphaeroma rugicauda
Estuarine, Coastal and Shelf Science (1985) 20,105-l
16
Population Dynamics of the Estuarine Isopod Sphaeroma rugicauda
David
J. Heath
Department CO4 3SQ, Received
and Aziz A. Khazaeli
of Biology, U.K. 24 April
University
of Essex,
1983 and in revised
form
Wivenhoe
Park,
8 February
1984
Keywords: Isopoda; estuaries; population dynamics; ratios; mortality; seasonal variation; English coast
Coichester,
climatic
Essex
effects; sex
Population density, spatial distribution, size distribution, sex ratio and fecundity were studied in a population over a three-year period. Young are produced in the summer, overwinter, reproduce and then die. Population densities decrease due to mortality from March to June and increase due to natality from July to September. Climate has a significant effect on population density. An abnormally warm summer (1976) led to earlier breeding, reduced fecundity, faster growth and higher mortality of juveniles. This led to fewer, larger, breeding adults in 1977. Two years which were climatically similar showed similar population trends. Egg and offspring number were positively correlated with female size but differed between years. Brood pouch mortality was estimated at 17”,,. Marked changes in population sex ratio were shown to be artefacts due to differences in swimming activity of the sexes. Introduction Sphaerorna rugicauda Leach is a common saltmarsh isopod of British and European estuaries (Stephenson, 1929; West, 1964; Lejuez, 1966; Bishop, 1969; Harvey, 1969; Heath, 1975a). It has been the subject of several studies both in terms of ecophysiology (Baig, 1959; Heath, 1975a; Marsden, 1976; 1979) and ecological genetics (West, 1964; Bishop, 1969; Heath, 1974; 197%; Khazaeli & Heath, 1979), and although some of these authors touch on its population dynamics there has been little detailed work on this subject. This paper describes the annual and seasonal variation in population density, sex ratio, fecundity and spatial distribution in one population over a three year period.
Materials The
and methods
study
area
The population lived in an area of saltmarsh at the head of Alresford Creek (Essex, England, 51~49’N, 0‘59’E). The saltmarsh was bounded by higher agricultural land to one side and by the bare mud of the creek to the other. Although the height of the marsh above sealevel varied it could be divided conveniently into higher and lower regions, which comprised 60”,, and 30”,, of the total area (the remainder consisted of channels). “Present
address:
Genetics
Research
Centre,
P.O. Box 1132, Ahwaz,
Iran.
105 037%7714~‘851010105+
12 $03.00:0
0 1985 Academic
Press Inc. (London:
Limited
106
D. J. Heath & A. Khazaeli
N
J
0
F
M
A
M
J
J
A
s
0
Month
Figure 1. Transformed mean density (*95”,, confidence limits), November 1975-September 1978; A-A, 1975-1976; O-O, 1976-1977; D-D, 1977-1978. (No sample in March 1977).
Low regions were flooded by tides above 5.6 m in height at Sheerness,higher regions by tides of height 5.8 m. The dominant vegetation was Puccinellia maritima (Huds.) with a few patches of Aster tripolium (L.). Laterally the area was bounded by stands of Phragmites communis (Trin.) within which the isopodswere rare. Sampling
Population densities were estimated by removing square cores (10 cm x 10 cm). Thirteen coreswere taken at random from a rectangular study area (30 m x 20 m) of the saltmarsh. Samples were taken at approximately ten-day intervals except over the period 22 July 1977to 30 August 1977 when they were taken more frequently to investigate in detail the changes in juvenile population density over the breeding season. Higher and lower regions of the marsh were investigated separately asfollows, after it becameapparent that there were density differences between them. Three sites were chosen within the study area, each site consisting of a higher and a lower region. On seven dates between 24 May 1977 and 27 July 1977, 5 cores were taken at random from each of these six regions (3 sites x 2 regions) on each sampling date. After this, samplestaken from the whole study area in the normal course of density estimations were identified as either coming from high or low regions
and were treated
separately.
Animals
were extracted
from the cores
and the numbers recorded. Samples of animals marsh. Large numbers
were also taken with a fine mesh net as spring tides flooded the of animals can be caught in this way and these animals were sexed
and measured under a binocular microscope. Males and females can be distinguished when they are longer than 3.5 mm. From November animals in cores were also recorded. Full details Khazaeli (1980).
1978 to May 1979, the sex ratios of of these procedures are given by
Fecurzdit-y and brood pouch mortality
Females from a net sample were measured and eggs were dissected from the brood pouch.
Females
fertilized
in the wild
were measured
and allowed
to release their
young
Population
Dvnamics of the Estuarine Isopod
107
. I\I \ j\ II ‘% I! “,.
J
J
Figure 2. Transformed ( ) regions of the three
TABLE
I, Comparisons
mean density (*95”,, sites, a, b and c.
of densities
Comparison
within
Month
confidence
limits)
and between
sites
t-P
P
?f
Betzueeu regims,‘withirr sites Site a: low and high Site b: low and high Site c: low and high
7 7
1.5
7
8.5 0
<0.05 < 0.05 < om
0 5
< 0.05 10.05
18.5
NS
Betwetx 1020regions of.rirrs 7 7 7
Site a:site b Site a,‘sitr c Site b;site c
Between high regions of sites 7 7 7
Site atsite b Site a:sirc c Site b,‘sire c “Number
of samples.
‘Mann-Whitney
0.5 0 0 statistic
<0.05 <0.05 10.05
at low (0)
and high
108
D.
3. Heath
& A. Khazaeli
S
Figure 3. Transformed and high (~ 1) regions, October.
0
N
mean monthly July 1977-July
0
M
A
M
J Month
density (i 95”,, confidence limits) at low ( n ) 1978. The broken lines indicate no sample for
in the laboratory. Brood pouch mortality was estimated by comparing the number of eggscarried with the number of young released, after correcting for any difference in average size of females. Results Population
density
The variance : mean ratio was greater than one for all samples,implying that the animals were contagiously distributed. To obtain confidence limits, the data have been transformed using the transformation log (x+ 1) (Elliott, 1971). All the original data can be found in Khazaeli (1980). Over the autumn and winter (September-April) there was little in the way of density change (Figure 1). There was a marked decreasein density from April to June and July in all three years. From June/July to September the densities increased to maximum values in July 1976 and in September 1977 and 1978. There were minor differences in timing and major differences in absolute densities between years. In particular densities increased slightly earlier in summer 1976, but peak densities were lower in late summer of this year compared to 1977 and 1978. The high late summer densities in 1977 were followed by autumn and winter densities which were uniformly higher than those in autumn 1975and autumn 1976. Mean population densities were lowest in the higher regions of the marsh (Figure 2) for the May-July period in 1977. For the seven dates differences between regions were significant, aswere differences between sites(Table 1). Site a waslower than site b which was lower than site c. Densities in low regions of the marsh were greater in late summer 1977and early summer 1978 (Figure 3). In the winter the higher areasof the marsh had the greatest densities.
Population
Dynamics
of the Estuarine
109
Isopod
The increase in population density in July and August coincides with the period when the young are released. Data for adults ( > 3.5 mm) and juvenile population densities are plotted separately for 1976 and 1977 (Figures 4 and 5). Adult densities decline steadily from May to August in 1976 (Figure 4) with a rapid increase in density of juveniles from mid- June to mid- July. The numbers of juveniles then fell by mid-August. This is unlikely to be due to recruitment to the adult section of the population since adult densities did not increase at this time. This suggested that perhaps juveniles were dying and this was investigated in more detail in 1977. Adult densities remained constant over this period while juvenile densities increased (Figure 5). This increase was correlated with the tidal cycle. Density increased abruptly over the period of spring tides (height > 5.7 m) in late June early August. Over the subsequent period of neap tides there was no increase in density. The density appeared to rise further in late August but with no clear relationship to tidal cycle. There was no decrease in juvenile density in 1977 unlike that observed in 1976.
M
Figure 4. Transformed juveniles (A) in summer
J
J
density 1976.
(&95”,,
A
confidence
Month
limits)
of the adults
(A)
and
Size distribution The data for the three years show marked similarities (Figure 6). Over the winter period, from November to March the average size did not change appreciably although there was some indication that the smallest size classes disappear. After March the average size increased until June and the young were released in June and July. The adults which had bred became much less common and by September they had disappeared from the population. The generations were therefore non-overlapping. The juveniles grew from July to October and then growth ceased over the winter. In the summer of 1978 juveniles were released later than in the other two years. Size of juveniles increased more rapidly in the summer of 1976 than in I977 and this was reflected in larger sizes of overwintering adults and breeding adults in 1977.
110
D. J. Heath
& A. Khazaeli
M
22 25 28 II I
J
6 P 12 II
A
18 ,I *a 2, 10
5
20 Day
i’
Month
Figure 5. Transformed mean density (*95”,, confidence limits) of adults (a) and juveniles (b) in summer 1977. Figure (c) shows the pattern of tidal cycle (stippled area height of tide > 5.7 m, and plain area between horizonral bars height of tide between 5.5-5.7 m).
Sex ratio The percentage of males was estimated from samples of swimming animals for three years (solid lines in Figure 7) and from core samples for one year (broken line in Figure 7). After June 1978 the number of adult animals in core samples was too low for meaningful estimates to be obtained. From November until April, sex ratios (OC1males) in both net and core samples were around 35”,, . There was some indication that over this period males became less common (Khazaeli, 1980). For the period November 1977 to June 1978 when both net and core samples were available sex ratios were compared by pairing each net sample with the core sample closest to it in time. There were no significant differences over the November-April period (Table 2). After April the sex ratio fluctuated markedly. In each year the percentage of males fell in late May or early June-this being most marked in 1978. In late June and early July the percentage of
Population
Dynamics
of the Estuarine
1976
111
Isopod
-77
Feb
SeP
act
Figure
6. Monthly
size class distribution
in three years,
November
1975August
1978.
males rose to values in excess of 90”,, before it fell rapidly in August to around 15”,, . It then rose again in September to the typical winter level. Such marked changes over such short time periods suggested a behavioural cause rather than real changes in the population. Sex ratios in net and core samples were significantly different over this period with the percentage of males much lower in the latter. A simple experiment was devised to test for differences in swimming activity between the sexes. Equal numbers of males and females were taken from the wild and placed in a tank of seawater. A square frame
112
D.J. Heath &A.
Khazaeli
0
NDJFMAMJJAS
Figure 7. Percentage of males amongst mature individuals 1975-August 1978; APA, 1975-1976; .~.,197&1977; and core samples (U---n, November 1977-June 1978).
TABLE 2. Comparison
Month
in net samples n -m,
(November 1977-1978)
of the sex ratio in net and core samples
Date Core sample
Net sample
23 2 23 16 6 7 9 17 3 15
16 9 24 22 9 11 8 28 7 26
Nov Dee Jan Feb Mar Apr May May Jun Jun
1977 1977 1978 1978 1978 1978 1978 1978 1978 1978
Nov Dee Jan Feb Mar Apr May May Jun Jun
1977 1977 1978 1978 1978 1978 1978 1978 1978 1978
%2,1,
P
1.25 0.12 2.76 3.82 1.44 042 2.24 72.66 28.25 271.40
NS NS NS NS NS NS NS -co.001
was suspended in the water near the surface and any animal swimming through this frame was caught, sexed and returned to the tank. This was repeated on several different dates. The swimming activity of males increased relative to that of females over the early summer (Table 3). Fecundity and brood pouch mortality The relationship between female size and egg number was investigated in 1976 and 1977, and between female size and young produced in 1976. The number of eggs carried was
Population
TABLE
Dynamics
of the Estuarine
3. The swimming activity of malesand femalesin the laboratory Number swimming male
Date 17 4 13 8 17 28 7 26
Jun 1977 Aug
1977
Apr 1978 May May May Jun Jun
113
Isopod
1978 1978 1978 1978 1978
100 24 51 77 81 80 79 72
female 47 26 49 52 32 41 40 12
Males (“,,) 68.02 48.00 51.00 59.69 71.68 66.11 66-39 85.71
X2,,) 19.11 0.08 0.04 4.84 21.25 12.57 12.78 42.86
P < 0.001 NS NS < 0.05
positively correlated with female size in both years (Figure 8). There was no significant difference between the slopes of the lines but the intercepts were significantly different (P
114
0.3. Heath
&A.
Khazaeli
70
8
,,,’,’
t
/..I
Figure 8. The relationship between female size and number 1977 (B) and female size and number of young in 1976 (A2). size distributions of females. Regression lines: Number
of eggs on female
(data points
Number
omitted
of young
size:
1976, for clarity) 1977, on female 1976,
of eggs for 1976 {Al) and The histograms show the
v = -46.03
+ 16.97x,
Al,
y = -38.89
+ 16?3x,
B.
size: y=
-65.77+
19.39~0,
A2.
Reproductive output is linearly related to body length a feature common to many isopods both aquatic and terrestrial e.g. Sphaeroma (Betz, 1980), Dynamze bidentata (Holdich, 1968), Idotea chelipes (Betz, 1974) and Philoscia IEUSCOYUWZ (Sunderland et al., 1976). Brood pouch mortality was estimated at 16,99O,, for 1976, a figure which lies within the range reported for similar species, although this characteristic varies widely within and between species. Kinne (1954) observed slight brood pouch mortality in
Population
Dynamics
of the Estuarine
115
Isopod
S. hookeri while Jensen (1955) observed none. Betz (1980) found no evidence of it in rugicauda or hook& whereas Schutz (1963) gives an average figure of 36”,, for hookeri from the Nord-Ostsee-Kanal in North Germany. In D. bidentata Holdich (1968) arrived at a figure of 36”,, while Betz (1974) described a reduction (unquantified) in embryo numbers during development in Zdotea chelipes. It seems reasonable to suggest that this characteristic will be sensitive to environmental factors so that differences between populations and between years are to be expected. The sex ratio outside the breeding season shows a preponderance of females which seems to be characteristic of other marine/brackish water isopods (see Betz, 1974; 1980; Jensen, 1955). In the breeding season sex ratios are modified by differences in the swimming activity of the sexes which affect their probabilities of capture in net samples. Males swim more readily than females early in the summer but not after young have been released, accounting for the generally high frequency of males. The sharp decline in male frequency in late May probably arises because of pairing. Since males are always less common than females the frequency of males swimming will decrease as pairs form prior to copulation (if all males were paired with females there would still be some unpaired females and the frequency of swimming males would be zero). After mating male frequency increases (presumably because gravid females are less active) and it then decreases rapidly as (a) males die (b) females start to swim after releasing young. If this is the correct interpretation and such effects are common in isopods then sex ratio data must be interpreted carefully in the light of the season and the sampling method. References Baig,
M. M. 1959 The morphology, ecology, reproduction and life cycle of S. riLggicuuda (Leach). Unpublished M.Sc. thesis, University of Liverpool. Betz, K. 1974 Phanologie, Reproduktion und Wachstum der Valviferen Assel Idotea chr’lipes (Pallas, 1976) in der Schlei. Kieler Meeresforschwtgen 30, 65-69. Betz, K. 1980 Sphaeroma rugicauda Leach, 1814 und S. hook& Leach, 1814 (Isopoda, Flabellifera):Grosse und Embryonalstadien in einer rugicauda/hookeri-Mischpopulation. Eine vergleichende Untersuchung. Mitteilwzgen aus dew Hambttrgischm zoologischen Museum uttd Imtitut 71,211-216. Bishop, J. A. 1969 Changes in genetic constitution of a population of Sphuerotrtu rugicauda (Crustacea : Isopoda). Evolution 23, 589-601. Elliott, J. M. 1971 Some methods for the statistical analysis of samples of benthic invertebrates. Frrsheuater Biological Assocmiott. Sciemjic Publication 25. Harvey, C. E. 1969 Breeding and distribution of Sphaeroma (Crustacea : Isopoda) in Britain. 3owrml of Animal Ecologwv 38, 399-406. Heath, D. J. 1974 Seasonal changes in frequency of the ‘yellow’ morph of the isopod Sphuerowa rugicwdu. Heredit.v 32,299-307. Heath, D. J. 197% Factors affecting temperature and salinity conditions on a Scottish salt-marsh, with notes on the ecology of Sphaeronm rugicauda (Leach). Archiv fiir Hydrobiologie 1,76-89. Heath, D. J. 19756 Geographical variation in populations of the polymorphic isopod, Sphaeronm rugicaudu. Heredit))
35,99-107.
Holdich, D. M. 1968 Reproduction, growth 3ourmzl oj.Zoology 156, 137-153. Jensen, J. I’. 1955 Biological observations Mrddrlelsrrfru
Damk
mzturhistorisk
Fore&g
and bionomics on the
isopod
i Kjobrnhnvrr
of Dymwtew Spharronta
469-546.
(Leach).
hookeri
117,305-339. isopod, Spharromu
Khazaeli, A. A. 1980 Ecological genetics of the polymorphic thesis, University of Essex. Khazaeli, A. A. & Heath, D. J, 1979 Colour polymorphism, selection Spharroma rugicauda (Leach). Heredity 41, 187-199. Kinne, 0. 1954 Eidonomie, Anatomie und Lebenszyklus van Sphaeroma Mreresjwschungen 10, 10@120. Lejuez, R. 1966 Comparison morphologique, biologique et genetique Sphaeromu Latreille (Isopodes Flabelliferes). Archives de Zoologie
(Crustacea
bidrntata
L’idemkabeiigc
(Leach).
rrrgicuttdu
and the sex ratio hookeri
Leach
de quelques, Experivtextal
: Isopoda).
Ph.D.
in the isopod
(Isopoda). especes
Kicler
du genre
et Generule
107,
116
D.
3.
Heath
6 A. Khazaeli
Marsden, I. D. 1976 Effect of temperature on the microdistribution of the isopod Sphaerotna rtcgicaudu from a salt-marsh habitat. Marine Biology 38, 117-128. Marsden, I. D. 1979 Seasonal oxygen consumption of the salt-marsh isopod Sphaeroma rugicauda. Marine Biology .51,329-337. Schutz, L. 1963 Die Beziehung zwischen Ei-, Embryonenzahl und Korpergrosse der Weibchen einiger Perarcarida aus dem Nord-Ostsee-Kanal. Zoologischer Anzeiger 171,291-302. Stephenson, K. 1929 Marine Crustacea, Isopoda and Tanaidacea. Zoology Faroes 24, l-23. Sunderland, K. D., Hassall, M. & Sutton, S. L. 1976 The population dynamics of Philoscia muscorum (Crustacea Oniscoidea) in a dune grassland ecosystem. jrournal of Animal Ecology 45,487-506. West, D. A. 1964 Polymorphism in the isopod, Sphaeroma rugicauda. Evolution 18,671-684.
16
Population Dynamics of the Estuarine Isopod Sphaeroma rugicauda
David
J. Heath
Department CO4 3SQ, Received
and Aziz A. Khazaeli
of Biology, U.K. 24 April
University
of Essex,
1983 and in revised
form
Wivenhoe
Park,
8 February
1984
Keywords: Isopoda; estuaries; population dynamics; ratios; mortality; seasonal variation; English coast
Coichester,
climatic
Essex
effects; sex
Population density, spatial distribution, size distribution, sex ratio and fecundity were studied in a population over a three-year period. Young are produced in the summer, overwinter, reproduce and then die. Population densities decrease due to mortality from March to June and increase due to natality from July to September. Climate has a significant effect on population density. An abnormally warm summer (1976) led to earlier breeding, reduced fecundity, faster growth and higher mortality of juveniles. This led to fewer, larger, breeding adults in 1977. Two years which were climatically similar showed similar population trends. Egg and offspring number were positively correlated with female size but differed between years. Brood pouch mortality was estimated at 17”,,. Marked changes in population sex ratio were shown to be artefacts due to differences in swimming activity of the sexes. Introduction Sphaerorna rugicauda Leach is a common saltmarsh isopod of British and European estuaries (Stephenson, 1929; West, 1964; Lejuez, 1966; Bishop, 1969; Harvey, 1969; Heath, 1975a). It has been the subject of several studies both in terms of ecophysiology (Baig, 1959; Heath, 1975a; Marsden, 1976; 1979) and ecological genetics (West, 1964; Bishop, 1969; Heath, 1974; 197%; Khazaeli & Heath, 1979), and although some of these authors touch on its population dynamics there has been little detailed work on this subject. This paper describes the annual and seasonal variation in population density, sex ratio, fecundity and spatial distribution in one population over a three year period.
Materials The
and methods
study
area
The population lived in an area of saltmarsh at the head of Alresford Creek (Essex, England, 51~49’N, 0‘59’E). The saltmarsh was bounded by higher agricultural land to one side and by the bare mud of the creek to the other. Although the height of the marsh above sealevel varied it could be divided conveniently into higher and lower regions, which comprised 60”,, and 30”,, of the total area (the remainder consisted of channels). “Present
address:
Genetics
Research
Centre,
P.O. Box 1132, Ahwaz,
Iran.
105 037%7714~‘851010105+
12 $03.00:0
0 1985 Academic
Press Inc. (London:
Limited
106
D. J. Heath & A. Khazaeli
N
J
0
F
M
A
M
J
J
A
s
0
Month
Figure 1. Transformed mean density (*95”,, confidence limits), November 1975-September 1978; A-A, 1975-1976; O-O, 1976-1977; D-D, 1977-1978. (No sample in March 1977).
Low regions were flooded by tides above 5.6 m in height at Sheerness,higher regions by tides of height 5.8 m. The dominant vegetation was Puccinellia maritima (Huds.) with a few patches of Aster tripolium (L.). Laterally the area was bounded by stands of Phragmites communis (Trin.) within which the isopodswere rare. Sampling
Population densities were estimated by removing square cores (10 cm x 10 cm). Thirteen coreswere taken at random from a rectangular study area (30 m x 20 m) of the saltmarsh. Samples were taken at approximately ten-day intervals except over the period 22 July 1977to 30 August 1977 when they were taken more frequently to investigate in detail the changes in juvenile population density over the breeding season. Higher and lower regions of the marsh were investigated separately asfollows, after it becameapparent that there were density differences between them. Three sites were chosen within the study area, each site consisting of a higher and a lower region. On seven dates between 24 May 1977 and 27 July 1977, 5 cores were taken at random from each of these six regions (3 sites x 2 regions) on each sampling date. After this, samplestaken from the whole study area in the normal course of density estimations were identified as either coming from high or low regions
and were treated
separately.
Animals
were extracted
from the cores
and the numbers recorded. Samples of animals marsh. Large numbers
were also taken with a fine mesh net as spring tides flooded the of animals can be caught in this way and these animals were sexed
and measured under a binocular microscope. Males and females can be distinguished when they are longer than 3.5 mm. From November animals in cores were also recorded. Full details Khazaeli (1980).
1978 to May 1979, the sex ratios of of these procedures are given by
Fecurzdit-y and brood pouch mortality
Females from a net sample were measured and eggs were dissected from the brood pouch.
Females
fertilized
in the wild
were measured
and allowed
to release their
young
Population
Dvnamics of the Estuarine Isopod
107
. I\I \ j\ II ‘% I! “,.
J
J
Figure 2. Transformed ( ) regions of the three
TABLE
I, Comparisons
mean density (*95”,, sites, a, b and c.
of densities
Comparison
within
Month
confidence
limits)
and between
sites
t-P
P
?f
Betzueeu regims,‘withirr sites Site a: low and high Site b: low and high Site c: low and high
7 7
1.5
7
8.5 0
<0.05 < 0.05 < om
0 5
< 0.05 10.05
18.5
NS
Betwetx 1020regions of.rirrs 7 7 7
Site a:site b Site a,‘sitr c Site b;site c
Between high regions of sites 7 7 7
Site atsite b Site a:sirc c Site b,‘sire c “Number
of samples.
‘Mann-Whitney
0.5 0 0 statistic
<0.05 <0.05 10.05
at low (0)
and high
108
D.
3. Heath
& A. Khazaeli
S
Figure 3. Transformed and high (~ 1) regions, October.
0
N
mean monthly July 1977-July
0
M
A
M
J Month
density (i 95”,, confidence limits) at low ( n ) 1978. The broken lines indicate no sample for
in the laboratory. Brood pouch mortality was estimated by comparing the number of eggscarried with the number of young released, after correcting for any difference in average size of females. Results Population
density
The variance : mean ratio was greater than one for all samples,implying that the animals were contagiously distributed. To obtain confidence limits, the data have been transformed using the transformation log (x+ 1) (Elliott, 1971). All the original data can be found in Khazaeli (1980). Over the autumn and winter (September-April) there was little in the way of density change (Figure 1). There was a marked decreasein density from April to June and July in all three years. From June/July to September the densities increased to maximum values in July 1976 and in September 1977 and 1978. There were minor differences in timing and major differences in absolute densities between years. In particular densities increased slightly earlier in summer 1976, but peak densities were lower in late summer of this year compared to 1977 and 1978. The high late summer densities in 1977 were followed by autumn and winter densities which were uniformly higher than those in autumn 1975and autumn 1976. Mean population densities were lowest in the higher regions of the marsh (Figure 2) for the May-July period in 1977. For the seven dates differences between regions were significant, aswere differences between sites(Table 1). Site a waslower than site b which was lower than site c. Densities in low regions of the marsh were greater in late summer 1977and early summer 1978 (Figure 3). In the winter the higher areasof the marsh had the greatest densities.
Population
Dynamics
of the Estuarine
109
Isopod
The increase in population density in July and August coincides with the period when the young are released. Data for adults ( > 3.5 mm) and juvenile population densities are plotted separately for 1976 and 1977 (Figures 4 and 5). Adult densities decline steadily from May to August in 1976 (Figure 4) with a rapid increase in density of juveniles from mid- June to mid- July. The numbers of juveniles then fell by mid-August. This is unlikely to be due to recruitment to the adult section of the population since adult densities did not increase at this time. This suggested that perhaps juveniles were dying and this was investigated in more detail in 1977. Adult densities remained constant over this period while juvenile densities increased (Figure 5). This increase was correlated with the tidal cycle. Density increased abruptly over the period of spring tides (height > 5.7 m) in late June early August. Over the subsequent period of neap tides there was no increase in density. The density appeared to rise further in late August but with no clear relationship to tidal cycle. There was no decrease in juvenile density in 1977 unlike that observed in 1976.
M
Figure 4. Transformed juveniles (A) in summer
J
J
density 1976.
(&95”,,
A
confidence
Month
limits)
of the adults
(A)
and
Size distribution The data for the three years show marked similarities (Figure 6). Over the winter period, from November to March the average size did not change appreciably although there was some indication that the smallest size classes disappear. After March the average size increased until June and the young were released in June and July. The adults which had bred became much less common and by September they had disappeared from the population. The generations were therefore non-overlapping. The juveniles grew from July to October and then growth ceased over the winter. In the summer of 1978 juveniles were released later than in the other two years. Size of juveniles increased more rapidly in the summer of 1976 than in I977 and this was reflected in larger sizes of overwintering adults and breeding adults in 1977.
110
D. J. Heath
& A. Khazaeli
M
22 25 28 II I
J
6 P 12 II
A
18 ,I *a 2, 10
5
20 Day
i’
Month
Figure 5. Transformed mean density (*95”,, confidence limits) of adults (a) and juveniles (b) in summer 1977. Figure (c) shows the pattern of tidal cycle (stippled area height of tide > 5.7 m, and plain area between horizonral bars height of tide between 5.5-5.7 m).
Sex ratio The percentage of males was estimated from samples of swimming animals for three years (solid lines in Figure 7) and from core samples for one year (broken line in Figure 7). After June 1978 the number of adult animals in core samples was too low for meaningful estimates to be obtained. From November until April, sex ratios (OC1males) in both net and core samples were around 35”,, . There was some indication that over this period males became less common (Khazaeli, 1980). For the period November 1977 to June 1978 when both net and core samples were available sex ratios were compared by pairing each net sample with the core sample closest to it in time. There were no significant differences over the November-April period (Table 2). After April the sex ratio fluctuated markedly. In each year the percentage of males fell in late May or early June-this being most marked in 1978. In late June and early July the percentage of
Population
Dynamics
of the Estuarine
1976
111
Isopod
-77
Feb
SeP
act
Figure
6. Monthly
size class distribution
in three years,
November
1975August
1978.
males rose to values in excess of 90”,, before it fell rapidly in August to around 15”,, . It then rose again in September to the typical winter level. Such marked changes over such short time periods suggested a behavioural cause rather than real changes in the population. Sex ratios in net and core samples were significantly different over this period with the percentage of males much lower in the latter. A simple experiment was devised to test for differences in swimming activity between the sexes. Equal numbers of males and females were taken from the wild and placed in a tank of seawater. A square frame
112
D.J. Heath &A.
Khazaeli
0
NDJFMAMJJAS
Figure 7. Percentage of males amongst mature individuals 1975-August 1978; APA, 1975-1976; .~.,197&1977; and core samples (U---n, November 1977-June 1978).
TABLE 2. Comparison
Month
in net samples n -m,
(November 1977-1978)
of the sex ratio in net and core samples
Date Core sample
Net sample
23 2 23 16 6 7 9 17 3 15
16 9 24 22 9 11 8 28 7 26
Nov Dee Jan Feb Mar Apr May May Jun Jun
1977 1977 1978 1978 1978 1978 1978 1978 1978 1978
Nov Dee Jan Feb Mar Apr May May Jun Jun
1977 1977 1978 1978 1978 1978 1978 1978 1978 1978
%2,1,
P
1.25 0.12 2.76 3.82 1.44 042 2.24 72.66 28.25 271.40
NS NS NS NS NS NS NS -co.001
was suspended in the water near the surface and any animal swimming through this frame was caught, sexed and returned to the tank. This was repeated on several different dates. The swimming activity of males increased relative to that of females over the early summer (Table 3). Fecundity and brood pouch mortality The relationship between female size and egg number was investigated in 1976 and 1977, and between female size and young produced in 1976. The number of eggs carried was
Population
TABLE
Dynamics
of the Estuarine
3. The swimming activity of malesand femalesin the laboratory Number swimming male
Date 17 4 13 8 17 28 7 26
Jun 1977 Aug
1977
Apr 1978 May May May Jun Jun
113
Isopod
1978 1978 1978 1978 1978
100 24 51 77 81 80 79 72
female 47 26 49 52 32 41 40 12
Males (“,,) 68.02 48.00 51.00 59.69 71.68 66.11 66-39 85.71
X2,,) 19.11 0.08 0.04 4.84 21.25 12.57 12.78 42.86
P < 0.001 NS NS < 0.05
positively correlated with female size in both years (Figure 8). There was no significant difference between the slopes of the lines but the intercepts were significantly different (P
114
0.3. Heath
&A.
Khazaeli
70
8
,,,’,’
t
/..I
Figure 8. The relationship between female size and number 1977 (B) and female size and number of young in 1976 (A2). size distributions of females. Regression lines: Number
of eggs on female
(data points
Number
omitted
of young
size:
1976, for clarity) 1977, on female 1976,
of eggs for 1976 {Al) and The histograms show the
v = -46.03
+ 16.97x,
Al,
y = -38.89
+ 16?3x,
B.
size: y=
-65.77+
19.39~0,
A2.
Reproductive output is linearly related to body length a feature common to many isopods both aquatic and terrestrial e.g. Sphaeroma (Betz, 1980), Dynamze bidentata (Holdich, 1968), Idotea chelipes (Betz, 1974) and Philoscia IEUSCOYUWZ (Sunderland et al., 1976). Brood pouch mortality was estimated at 16,99O,, for 1976, a figure which lies within the range reported for similar species, although this characteristic varies widely within and between species. Kinne (1954) observed slight brood pouch mortality in
Population
Dynamics
of the Estuarine
115
Isopod
S. hookeri while Jensen (1955) observed none. Betz (1980) found no evidence of it in rugicauda or hook& whereas Schutz (1963) gives an average figure of 36”,, for hookeri from the Nord-Ostsee-Kanal in North Germany. In D. bidentata Holdich (1968) arrived at a figure of 36”,, while Betz (1974) described a reduction (unquantified) in embryo numbers during development in Zdotea chelipes. It seems reasonable to suggest that this characteristic will be sensitive to environmental factors so that differences between populations and between years are to be expected. The sex ratio outside the breeding season shows a preponderance of females which seems to be characteristic of other marine/brackish water isopods (see Betz, 1974; 1980; Jensen, 1955). In the breeding season sex ratios are modified by differences in the swimming activity of the sexes which affect their probabilities of capture in net samples. Males swim more readily than females early in the summer but not after young have been released, accounting for the generally high frequency of males. The sharp decline in male frequency in late May probably arises because of pairing. Since males are always less common than females the frequency of males swimming will decrease as pairs form prior to copulation (if all males were paired with females there would still be some unpaired females and the frequency of swimming males would be zero). After mating male frequency increases (presumably because gravid females are less active) and it then decreases rapidly as (a) males die (b) females start to swim after releasing young. If this is the correct interpretation and such effects are common in isopods then sex ratio data must be interpreted carefully in the light of the season and the sampling method. References Baig,
M. M. 1959 The morphology, ecology, reproduction and life cycle of S. riLggicuuda (Leach). Unpublished M.Sc. thesis, University of Liverpool. Betz, K. 1974 Phanologie, Reproduktion und Wachstum der Valviferen Assel Idotea chr’lipes (Pallas, 1976) in der Schlei. Kieler Meeresforschwtgen 30, 65-69. Betz, K. 1980 Sphaeroma rugicauda Leach, 1814 und S. hook& Leach, 1814 (Isopoda, Flabellifera):Grosse und Embryonalstadien in einer rugicauda/hookeri-Mischpopulation. Eine vergleichende Untersuchung. Mitteilwzgen aus dew Hambttrgischm zoologischen Museum uttd Imtitut 71,211-216. Bishop, J. A. 1969 Changes in genetic constitution of a population of Sphuerotrtu rugicauda (Crustacea : Isopoda). Evolution 23, 589-601. Elliott, J. M. 1971 Some methods for the statistical analysis of samples of benthic invertebrates. Frrsheuater Biological Assocmiott. Sciemjic Publication 25. Harvey, C. E. 1969 Breeding and distribution of Sphaeroma (Crustacea : Isopoda) in Britain. 3owrml of Animal Ecologwv 38, 399-406. Heath, D. J. 1974 Seasonal changes in frequency of the ‘yellow’ morph of the isopod Sphuerowa rugicwdu. Heredit.v 32,299-307. Heath, D. J. 197% Factors affecting temperature and salinity conditions on a Scottish salt-marsh, with notes on the ecology of Sphaeronm rugicauda (Leach). Archiv fiir Hydrobiologie 1,76-89. Heath, D. J. 19756 Geographical variation in populations of the polymorphic isopod, Sphaeronm rugicaudu. Heredit))
35,99-107.
Holdich, D. M. 1968 Reproduction, growth 3ourmzl oj.Zoology 156, 137-153. Jensen, J. I’. 1955 Biological observations Mrddrlelsrrfru
Damk
mzturhistorisk
Fore&g
and bionomics on the
isopod
i Kjobrnhnvrr
of Dymwtew Spharronta
469-546.
(Leach).
hookeri
117,305-339. isopod, Spharromu
Khazaeli, A. A. 1980 Ecological genetics of the polymorphic thesis, University of Essex. Khazaeli, A. A. & Heath, D. J, 1979 Colour polymorphism, selection Spharroma rugicauda (Leach). Heredity 41, 187-199. Kinne, 0. 1954 Eidonomie, Anatomie und Lebenszyklus van Sphaeroma Mreresjwschungen 10, 10@120. Lejuez, R. 1966 Comparison morphologique, biologique et genetique Sphaeromu Latreille (Isopodes Flabelliferes). Archives de Zoologie
(Crustacea
bidrntata
L’idemkabeiigc
(Leach).
rrrgicuttdu
and the sex ratio hookeri
Leach
de quelques, Experivtextal
: Isopoda).
Ph.D.
in the isopod
(Isopoda). especes
Kicler
du genre
et Generule
107,
116
D.
3.
Heath
6 A. Khazaeli
Marsden, I. D. 1976 Effect of temperature on the microdistribution of the isopod Sphaerotna rtcgicaudu from a salt-marsh habitat. Marine Biology 38, 117-128. Marsden, I. D. 1979 Seasonal oxygen consumption of the salt-marsh isopod Sphaeroma rugicauda. Marine Biology .51,329-337. Schutz, L. 1963 Die Beziehung zwischen Ei-, Embryonenzahl und Korpergrosse der Weibchen einiger Perarcarida aus dem Nord-Ostsee-Kanal. Zoologischer Anzeiger 171,291-302. Stephenson, K. 1929 Marine Crustacea, Isopoda and Tanaidacea. Zoology Faroes 24, l-23. Sunderland, K. D., Hassall, M. & Sutton, S. L. 1976 The population dynamics of Philoscia muscorum (Crustacea Oniscoidea) in a dune grassland ecosystem. jrournal of Animal Ecology 45,487-506. West, D. A. 1964 Polymorphism in the isopod, Sphaeroma rugicauda. Evolution 18,671-684.