J . Zool., Lond. (1991) 224,347-365

Seasonal changes in populations of three sympatric isopods in a Hong gong forest

H. H. T. MAI, D. DUDGEON' AND P. K. S. LAM**

'Department of Zoology, University of Hong Kong, Hong Kong zDepartment of Biology, Chinese University of.Hong Kong, Shatin, Hong Kong

(Accepted I 1 July 1990)

(With 10 figures in the text)

Data on the population dynamics of tropical isopods in general, and those inhabiting forests in particular, are scarce. Consequently, the population dynamics of three sympatric isopods, Burmoniscus ocellarus (Philosciidae), Formosillo raffaelei and Orodillo maculatw (Armadillidae), were studied at two neighbouring sites in a mixed forest in Hong Kong between March 1985 and December 1986. Isopod population densities varied with the species, site and season, with mean densities ranging from 100-150 m-2. Burmoniscus ocellarus and F. raffmlei had a single recruitment peak per year, while 0. maculatus had two. Results of the present study revealed that air temperature was the main factor explaining seasonal variations in population density, while rainfall exerted its effect with a two- to three-week timc-lag. depending on the species studied. Approximately 20% of Formosillo raffaelei and 0. macularus sampled were found infected by Rickerfsiella bacteria. The possible influence of pathogens, and other biotic factors, on the dynamics of the Hong Kong isopod populations was diicussed

Contents

Page Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347 Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . 348

Study area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348 Sampling procedure . . . . . . . . . . . . . . . . . . . . . . . . . . . 348 Data analysis.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 350

Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 350 Population dynamics of Burmoniscus ocelldtus . . . . . . . . . . . . . . . . . . Population dynamics of Formosillo raffaelei . . . . . . . . . . . . . . . . . . 35 1 Population dynamics of Orodillo maculatus . . . . . . . . . . . . . . . . . . 352

Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356 363

Influence of biological factors . . . . . . . . . . . . . . . . . . . . . . . . . 363 References . . . . . . . . . . . . . ! . . . . . . . . . . . . . . . . . . . . 364

350

Influence of climatic factors. . . . . . . . . . . . . . . . . . . . . . . . . .

Introduction

The population dynamics of temperate-zone isopods are affected by environmental factors such as daylength and temperature (Paris, 1963; McQueen & Carnio, 1974; McQueen, 1976~1, b, c;

*To whom correspondence should be addressed

347 0952-8369/91/007347 + 19 S03.00 0 1991 The Zoological Society of London

348 H . H . T. M A , D. DUDGEON AND P. K . S. LAM

McQueen & Steel, 1980; Davis, 1984; Warburg, Linsenmair & Bercovitz, 1984; Warburg, 1987; Miller & Cameron, 1987). Biotic influences including predation (Sutton, 1970; Sunderland & Sutton, 1980; Nair, I98 I), pathogenic and parasitic infections (Federici, 1984; Sassaman & Garthewaite, 1984; Hess & Poinar, 1985; Poinar & Paff, 1985; Shay et al., 1985; El-Aal & Holdich, 1987), and the availability of high-quality food (Rushton & Hassall, 1987) may also be important.

Studies of isopod populations have been undertaken mainly in temperate grassland habitats (e.g Sutton, 1968; Breymeyer & Brzozowska, 1970; Sunderland, Hassall & Sutton, 1976; Davis & Sutton, 1978; Hassall& Sutton, 1978; Hassall, 1983; Davis, 1984), and little comparable work has been undertaken in the tropics (Nair, 1978, 1981, 1984). Indeed, information on forest isopods in general, and tropical forest isopods in particular, is generally scarce, despite their importance in litter breakdown (Lam & Dudgeon, 1985a) and nutrient cycling. The present study records temporal variations in the abundance of three sympatric isopods at two sites in a Hong Kong forest, and relates these changes to environmental factors. In a later paper (Ma, Lam & Dudgeon, 1991), we compare the life-history variations within and between the three isopod species to explore the possible adaptive significance of these patterns. The three isopod species were Burmoniscus ocellatus (Verhoeff 1928) (Philosciidae), Formosillo raflaelei (Arcangeli 1927) (Armadillidae) and Orodillo maculatus Arcangeli 1952 (Armadillidae). To date, none of them has been the subject of ecological studies in Hong Kong or elsewhere.

Materials and methods

Study area

The study was undertaken in a secondary mixed broad-leaved evergreen forest on a north-facing gentle slope (about 15") on 'Hill above Belcher's', Hong Kong Island (22" 18' N, 114" 10' E) at an altitude of approximately 120 m. A list of common plant species and a detailed description of the general chemical and physical conditions of the study area are given by Lam & Dudgeon (19856) and Ma (1988). Within the study area, 2 adjacent sites (A and B) were investigated, which were separated by a concrete-lined conduit along which rain water drained. Site A had a closed canopy and was deeply shaded. The canopy at site B was broken and, in places, the litter layer was exposed to sunlight. This site experienced surface runoff of water during heavy rain.

Litter surface temperatures taken on each visit to the study site ranged from 12 "C in January 1986 to 29 "C in August 1986. Annual rainfall was 2191.4mm in 1985 and 2338.3 mm in 1986. Maximum daily precipitation (208.1 mm) was recorded on 25 June 1985 during Typhoon Hal. Monthly total rainfall during the study period was highest in July 1986 (547.3 mm). No rain was recorded during January 1986 (Fig. 1). Relative humidity ranged between 31 YO ( 5 January 1986) and 96% (9 April 1985). Moisture content of soil samples, collected during each visit to the sampling sites between September 1985 and November 1986, appeared to be higher at site A (mean=78-04%) than at site B (mean=74.53%) (Fig. I), but the difference was not statistically significant (2-sample I-test on arc-sine transformed data: I = 1.86, d.J = 21, P=O.O77).

Sampling procedure

Isopods were sampled at monthly intervals from February 1985 to November 1986, and at 2-week intervals during the breeding season (March-July 1985). Samples of leaf litter, together with loose top soil (approximately 2 cm deep), were collected from 16 'random' 25 x 25 cm quadrats at each of the 2 sites (A and B). Samples were taken between 09:30 and I1:30 h to reduce possible bias resulting from diurnal activity rhythms which are characteristic of some litter fauna (Cloudsley-Thompson, 1967).

POPULATION DYNAMICS O F HONG KONG ISOPODS

- 600 - E E v

I - - a C c .- 2 - a 0 r.

C

4-

4-

I z r"

1 0

349

E! 3 c E c i Q

L .- a

10

--- Relative humidit - .-

FIG. I . (a) Monthly mean relative humidity between' February 1985 and November 1986, and the soil moisture content of the study area between September 1985 and November 1986. (b) Monthly mean minimum, mean and mean maximum air temperature, and the monthly total rainfall between February 1985 and November 1986. [Temperature, rainfall and relative humidity data were obtained from the Hong Kong Royal Observatory reports (1985-86)].

Isopods were extracted from individual samples using Berlese funnels (Southwood, 1978), and counted. The isopods were killed by exposure to 95% ethanol vapour, so as to avoid rolling-up of conglobating species and stretching of the non-conglobating ones. Body length, from the anterior profrons to the end of the telson, was measured using a graticuled eyepiece on a stereomicroscope. As body length (BL) was linearly related to head width(HW)(r=0,99,n=58, P < O . O O I ) , thelatterwasused toestimateBLincaseswhere theprofronsor telsons had been damaged during collection. In addition to measurements of size, the sex of each individual was established (by the presence or absence of the male copulating organs, first and second pair of pleopods),

350 H . H . T. MA. D . DUDGEON AND P. K . S . LAM

and the presence of gravid females noted. All individuals were then oven-dried to constant weight ( f 0.1 mg) at 70 “C.

Data analysis

Analysis of population trends involved separation of sample populations, plotted on frequency histograms with a 0.2 mm size interval, into individual cohorts. Cohort separation involved following the growth of new recruits and the subsequent trends from those months with well-defined peaks in size-frequency histograms. We recognize that the method of interpretation of population trends employed here implies that juveniles born at the same time grow at a homogeneous rate. Animals in laboratory culture showed no clear signs of individual differences in growth rate, but such variation in the field may have confounded our interpretation. Nevertheless, the existence of well-defined peaks in the size-frequency histograms points to the existence of an ‘average’ growth rate for a cohort, albeit with some variation around the mean rate.

Calculation of Morisita’s Index of Aggregation (Poole, 1974) revealed that all 3 isopod species were contagiously distributed (Ma, 1988). Accordingly, population densities were loglo transformed to remove mean and variance correlations (Elliott, 1977) prior to data analysis. To uncover the effect of meteorological parameters on isopod population dynamics, the mean population density of each species on each date was correlated with prevailing temperature, rainfall and relative humidity. Time-lag correlation analyses and stepwise multiple-regression analyses were also performed on these parameters using the SPSS-X statistical package (Nie, 1983).

Results

Population dynamics of Burmoniscus ocellatus

Population densities were consistently higher a t site B (mean density 7.1 per 0.0625 m?) than a t site A (mean density 2.2 per 0,0625 m2) (Fig. 2). The density of B. ocellatus a t site A peaked during August 1985 and June 1986 while conspecifics a t site B reached maximum densities during October 1985 and August 1986. Mean population densities were positively correlated with weekly mean air temperature (P< 0.001) a t both sites (Table I). There was no significant correlation between population densities and weekly mean relative humidity (Table I). Stepwise multiple-regression analysis indicated that prevailing temperature was the meteorological factor explaining the

TABLE I Correlation roeficients of mean population density (no./0.0625 m2) of the four

Hong Kong isopods with prevailing meteorological factors

Weekly Weekly mean Weekly

mean air relative total Species temperature humidity rainfall

Burmoniscus (Site A) 0.716*** 0.3 I7 NS 0.480* ocella t us (Site B) 0.742*** -0.081 NS 0.136*** Formosillo (Site A) 0.812*** 0.295 NS 0.3 10 NS raffaelei (Site B) 0.677*** 0.247 NS 0.183 NS Orodillo (Site A) 0.346 NS 0‘050 NS -0.088 NS maculatus (Site B) 0.510** 0.012 NS -0.277 NS

~~ ~ ~~

Significance levels: NS Not significant; * P < 0.05; ** P < 0.01; *** P < 0.001

POPULATION DYNAMICS O F HONG KONG ISOPODS

Y

5 m ! I +

'0

s c s o

a

3 P 0

0 Site A 0 Site B 0 Site B

v)

2 - P

2 s

8

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.9 '

m 0 2. u)

'0

+

5 s c s o P 3 M A M J J A S O N D J F M A M J J A S O N D a 1985 1986 0 1985 1986

35 I

FIG. 2 . Seasonal variations in the densities of Eurmoniscus ocellutus at site A (April 198550ctober 1986) and site B (February 1985-November 1986). Vertical lines are+ 1 S.E.

observed variations in abundance at both sites even if a time-lag (three weeks at site A and two weeks at site B) was allowed for other factors to exert their influence (Table 11).

Burmoniscus ocellatus bred between February and September, with a major recruitment peak in April/May, and a minor one in July. Juveniles (mean body length 1.4 mm) were first released in April, and they grew rapidly to reach 6 mm by August when they bred (Fig. 3). Breeding individuals grew slowly while reproducing in late summer (August and September). A further period of slow growth, involving all individuals, followed during the winter (December to March). In 1986, gravid females began to appear in February and March at sites A and B, respectively (Fig. 3). Breeding continued until late summer as the early cohort-of-the-year joined the breeding group (Figs 3 and 4). Most B. ocellatus isopods died during their second winter, giving an average life span of one-and-a-half to slightly less than two years. However, a few individuals might have survived the second winter and contributed to recruitment in the following year, yielding a maximum of about three broods in their lifetime. These isopods had a maximum body length of 10.9 mm, and a maximum weight of 13.0 mg.

Population dynamics of Formosillo raffaelei

Population densities were higher at site A (mean density 9.2 per 0.0625 m2) than at site B (mean density 1.0 per 0.0625 m') (Fig. 5). Densities of F. rafaelei peaked during the summer (June- August) and autumn (October-November) in both 1985 and 1986 (Fig. 5). Mean population densities were positively correlated with weekly mean air temperature at both sites, but not with weekly total rainfall or weekly mean relative humidity (Table I). Stepwise multiple-regression analysis indicated that temperature was the meteorological factor explaining the observed

352 H . H. T . M A , D. DUDGEON A N D P. K. S . LAM

TABLE 11

Results of stepwise multiple-regression anul.vsis of weekly meteorological para- meters against mean densities of Burmoniscus ocellatus from April I985 10

October 1986. Only the best-fitting models ure presented

Variable r' F dtJ

Site A with prevailing weather Temperature 0,512 16.78*** 1.16

Temperature +Rainfall +Relative humidity 0.588 6.67.. 3,14

time lag of three weeks Temperature 0.577 21,82*** 1.16

Temperature +Rainfall +Relative humidity 0.644 8.43** 3.14

Site B with prevailing weather Temperature 0.551 24.53*** 1.20

Temperature +Rainfall +Relative humidity 0.688 13,21*** 3,18

time lag of two weeks Temperature 0.781 71.24*** 1.20

Temperat ure +Rainfall +Relative humidity 0.794 23.17*** 3.18

Significance levels: ** P<O.OI; *** P<0401

variations at both sites. However, weekly total rainfall became the main factor exp in ing the observed variations at site B if a two-week time-lag in its effect was allowed (Table 111).

Recruits (body length 1.7 mm) first entered the population in June, but the major period of recruitment was in September (Fig. 6). Juveniles did not reproduce until they were 13 months old. After a slow growth phase in winter (December-April), juveniles attained a body length of 7-8 mm by August and September (Fig. 7). They then bred and contributed to the major peak of recruitment. During their second year of life, individuals may have bred twice, once in late spring (April), and again in autumn (October). A few individuals survived a third winter, and bred again (during late spring) in their third year of life, yielding a maximum of four broods per lifetime. The mean life span was about three years (Figs 6 and 7). Formosillo raffaeleicould have a maximum life span of up to 40 (site A) or 48 (sitc B) months, and a maximum body length of 14.0 mm (body weight 50.4 mg).

Population dynamics of' Orodillo maculatus

Population densities at both sites A (6.1 per 0.0625 m2) and B (6.5 per 0.0625 m2) were similar (Fig. 8). The temporal pattern of abundance was bimodal with a decline in population density at

POPULATION D Y N A M I C S OF H O N G KONG ISOPODS 353

Burmoniscus ocellatus

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3/7/85 20 20, 85a n=95

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Body length (mrn)

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17/2/86 85 n=59

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24/6/86 10

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2;*=182

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10

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10 7/1/86

23--'=4Y=g4 10

83 14/3/86

203 A n=26

10 0 ~ / 5 / 8 6

10' 30Rl86 n=271

10 8q 28/11/86 n= 62

10

Body length (rnm)

FIG. 3. Size-frequency histograms of Burmoniscus ocellafus at site A (April 1985-October 1986) and site B (February 1985-November 1986). Females and immatures are shown above and males below the middle line. Black sections of the bars indicate females with marsupia. Numbers represent the year of birth ofeach cohort. Sampling date and sample size (n ) are given for each histogram.

354 H. H . T. MA. D . D U D G E O N A N D P. K . S . LAM

(a) Burmoniscus ocellatus

I I

M A M J J A S O N D J F M A M J J A S O N D 1985 1986

FIG. 4 . Growth curves with mean body length f I S.D. of each cohort of Burmoniscus ocellclrus at (a) site A (April 1985 October 1986) and (b) site B (February 1985-November 1986). Numbers represent the year of birth of each cohort.

POPULATION DYNAMICS OF HONG KONG ISOPODS

TABLE 111 Resulis of siepwise muliiple-regression analysis of weekly meteorological para- meters againsi mean densiiies of Formosillo raffaelei from April 1985 to October

1986. Only ihe best-fiiiing models are presenied

Variable r2 F dJ

Site A with prevailing weather Temperature 0.659 36.77*** 1.19

~~

Temperature +Rainfall +Relative humidity 0.678 I1.95*** 3,17

~

time lag of three weeks Temperature 0.637 33,37*** 1.19

Temperature +Rainfall +Relative humidity 0.648 10.42*** 3,17

Site B with prevailing weather Temperature 0.459 16.96*** 1.20

Temperature +Rainfall +Relative humidity 0.466 5.24'. 3.18

time lag of two weeks Rainfall 0.458 16.93*** 1,20

Rainfall +Temperature +Relative humidity 0,524 660*** 3,18

355

Significance levels: **f < O . O l ; ***P<O.001

the end of summer. Two peaks of recruitment, one in the summer months (April-July) and the other in the autumn and early winter (October-December), were noted.

Mean population densities were correlated with weekly mean air temperature at site B only, but not with weekly total rainfall or weekly mean relative humidity at either site (Table I). Stepwise multiple-regression analysis indicated that temperature was the main meteorological factor explaining the variance in population density, while rainfall acted as a co-factor in explaining the observed fluctuations in abundance at site B (Table IV). If a two-week time-lag in their effects was allowed, weekly total rainfall was the factor explaining the observed variations at site B. None of the three meteorological factors was able to explain the observed variations in mean population density at site A (Table IV).

Juveniles of I .7 mm body length entered the population in late April (Fig. 9). They were able to produce their first brood in about 12 months when they had reached a body length of6-7 mm (Fig. 10). Thus, excepting a few individuals which reproduced in October, most of the April cohort reproduced in early summer of the following year with the late cohort breeding during late summer of that year. In the following year, both cohorts bred twice (as early as February) before the onset of summer (June) and died. A few individuals might have survived and bred once more in late summer (September), giving a maximum of four boods per lifetime (Figs 9 and 10). The

356 H. H . T. MA, D. DUDGEON AND P. K. S. LAM

% I @Site A

1985 1986

FIG. 5. Seasonal variations in the densities of Formosillo ruffaelei at site A (March 1985-October 1986) and site B (February 1985-November 1986). Vertical lines are* 1 S.E.

population mainly comprised three year classes. Life span of this species averaged 2-3 years. Maximum recorded body length was 10.6 mm (body weight 14.4 mg).

Observations on the population dynamics of the study species have been summarized in Table V, which presents a comparison of life-history parameters of the three isopods.

Discussion

Isopod population densities vary according to the species and habitats under study. Paris & Pitelka (1962) found a density of 500 m-2 before the onset of recruitment for Armadillidium vulgare in the United States. For the same species, Al-Dabbagh & Block (1981) recorded 200-1000 m-2 in England. Sutton (1968) counted up to 2150 mP2 for the grassland species Trichoniscus pusillus but only 265 m-2 for co-occurring Philoscia muscorum. Saito (1969) recorded densities of 50-350 m-2 before the breeding season of three Japanese isopods. Shachak (1980) reported a density range of 0.1448 m-2 for the desert isopod Hemilepistus reaumuri, but Warburg, Linsenmair & Bercovitz (1984) believed that the population densities of this species may be up to 300-600 individuals per m2.

The average population density of each of the Hong Kong isopods ranged from 100-150 m-2 (with the exception of the low densities of Burmoniscus ocellatus at site A and Formosillo raflaelei

FIG. 6. Size-frequency histograms of Formosih ruflaelei at site A (March 1985-October 1986) and site B (February 1985-November 1986). Females and imrnatures are shown above and males below the middle line. Black sections of the bars indicate females with marsupia. Numbers represent the year of birth of each cohort. Sampling date and sample size (n) are given for each histogram.

POPULATION DYNAMICS 1

Fomosillo raffaelei Site A -

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1/5/85 n= 150

20 n=256

1/8/85 n=344 n=361

85b

10

10 10/7/86 10

86b n=263

7 O m h O D O N 7 7

10

DF HONG KONG ISOPODS

Site B

n=10

10/4/85

15/5/85 20 n=15

20 n=23

10 14/8/85

91 1 2/85 n=5

20& 0

401 11T1tf15 20 0

10 24/4/85 n=13

10 29/5/85 n=41 2;)

10 16/7/85

501 1712/88 801 8r 14/3/06

n=4 n-7

1 3/4/86 13/5/86 n=32 20

357

Body length (mm) FIG. 6

358 H . H . T. MA, D . DUDGEON AND P. K . S . LAM

(a) fomosillo raffaelei

POPULATION DYNAMICS OF HONG KONG ISOPODS 359

N-

v)

E

i - z c 3 a 8 8 B 6

.- b

.- 5

0 \

3

- 0

v) c 0, -0

c m 3 a 0

-

n

M A M J J A S O N D J F M A M J J A S O N D 1985 1986

F I G . 8 . Seasonal variations in the densities of Orodillo muculurus at site A (March 1985-October 1986) and site B (February 1985-November 1986). Vertical lines aref 1 S.E.

at site B), peak densities varying from 250-400 m-?. These population densities are comparable to values recorded for isopods in other parts of the world (see above), although higher densities have been obtained for investigations in habitats containing a single dominant species. In the present study, B. ocellatus and Orodillo macularus co-dominated at site B, while F. ragaelei and 0. maculutus co-dominated at site A. Available data do not permit us to explain this difference in species-abundance pat tern.

In siru observations indicated that some Formosillo raffaelei moved down into the soil during winter (cf. Davis, Hassall & Sutton, 1977), while Orodillo maculutus exhibited a tendency to climb on to tree trunks during the rainy season. Consequently, absolute densities of these isopods were sometimes difficult to determine and some of the data presented herein may be under-estimates. Vertical migration by isopods has been described by Brereton (1957) and Den Boer (1961) in the temperate region, but this phenomenon has not been reported from tropical regions (Warburg, Linsenmair & Bercovitz, 1984).

FIG. 7 . Growth curves with mean body length5 I S.D. of each cohort of Formosillo ruffuelei at site A (March 1985- October 1986) and site B (February 1985-November 1986). Numbers represent the year of birth of each cohort.

3 60 H. H. T. MA, D. DUDGEON AND P. K. S. LAM

Orodillo maculatus

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FIG. 9. Size-frequency histograms of Orodillu maculatus at site A (March 1985-October 1986) and site B (February 1985-November 1986). Females and immatures are shown above and males below the middle line. Black sections of the bars indicate females with marsupia. Numbers represent the year of birth ofeach cohort. Sampling date and sample size (n) are given for each histogram.

'4 POPULATION

Orodillo maculatus

Site A

DYNAMICS OF HONG KONG ISOPODS 36 1

FIG. 10. Growth curves with mean body lengthf 1 S.D. of each cohort of Orodillo maculatus at site A (March 1985- October 1986) and site B (February 1985-November 1986). Numbers represent the year of birth of each cohort.

362 H. H. T. MA. D. DUDGEON A N D P. K. S. LAM

TABLE I V Results of stepwise multiple-regression analysis of weekly meteorological para- meters against mean densities of Orodillo maculaius from April 1985 to October

1986. Only the best-Jirring models are presenred for site B ~~ ~

Variable ' rz F dJ

Site A with prevailing weather Temperature

+Rainfall +Relative humidity 0.169 1.15 NS 3,17

time lag of three weeks Temperature +Rainfall +Relative humidity 0.162 1.10 NS 3.17

Site B with prevailing weather Temperature 0.260 7.01* 1,20

Temperature +Rainfall 0400 6.34** 2,19

Temperature + Rainfall +Relative humidity 0.432 4.56* 3.18

-

time lag of two weeks Rainfall 0.342 10.38** 1.20

Rainfall +Temperature +Relative humidity 0.352 3.25* 3.18

~ ~

Significance levels: NS not significant; * P< 0.05; ** Pc0.01

TABLE V A summary of the life-history patterns of Burmoniseus orelhius, Formosillo raflaelei and

orodillo maculrrius

Burmoniscus Formosillo Orodillo ocellatus raffaelei maculatus

Time to first breeding 4 months 13 months 12 months Breeding period February- June- April-August and

September November October-February Brooding period 1-2 months 2 months 2 months Mean size ofjuveniles on release I .4 mm 1.7 mm 1.7 mm Minimum size at first breeding 6 mm 7 mm 6 mm Maximum size attained 10.9 mm 14.0 mm 10.6 mm Mean number of broods 2 3 3 Maximum number of broods 3 4 4 Mean life span 13 months 36 months 30 months Maximum life span 27 months 48 months 41 months

POPULATION DYNAMICS OF HONG KONG ISOPODS 363

Influence of climatic factors

Miller & Cameron ( I 987) proposed feedback models to explain the effects of temperature and rainfall in limiting Armadillidium uulgare populations in forest and grassland. They showed that temperature and rainfall were important factors accounting for up to 85% of the observed variation in isopod density, with temperature serving as the main factor in oak-forest habitats.

Temperature was the main factor explaining the observed variations in densities for all three Hong Kong isopod species. Stepwise multiple-regression analysis indicated that rainfall was less important at site A, but rainfall became the main factor for both armadillids at site B (but not at site A) if a time-lag in its effect was introduced. This difference may have been related to the more open canopy at site B, while the closed canopy at site A provided a more stable environment which ameliorated the effect of seasonal fluctuations in rainfall. The weekly mean air temperature was strongly correlated with mean population densities of all three species whether a time-lag effect was introduced or not. Temperatures during the weeks preceding sampling were also correlated with Burmoniscus ocellatus densities at sites A and B as well as the numbers of Formosillo ruflaelei and Orodillo maculatus at the former site. This effect probably results from the influence of temperature upon isopod growth and development rates, as well as initiation of reproduction (McQueen & Carnio, 1974; McQueen, 1976~; McQueen & Steel, 1980).

It is noteworthy that although temperature and rainfall appeared to have an influence on isopod densities, more data would be required to establish a causal relationship between density and the above meteorological factors. Clearly, isopod densities represent a balance between natality and mortality processes. The onset of breeding could be determined by day length cues, which may act in combination with temperature. Moreover, meteorological influences may not be simple linear functions but could exhibit threshold effects. Our simple linear regression models would not reveal such influences. Furthermore, the possible relationship between mortality and temperature has yet to be established.

Rushton & Hassall ( 1 987) have discussed the importance of high-quality food supplies in limiting isopod populations, while Miller & Cameron (1983, 1987) observed that the tannin- containing litter became a suitable isopod diet only after the winter and spring rains. Breakdown rates of Ficusfistulosa leaves in Hong Kong are positively correlated with prevailing temperature, rainfall and soil moisture content (Lam & Dudgeon, 19851). Although litter falls throughout the year in Hong Kong (Lam & Dudgeon, 19856), plant species differ in their litterfall phenology, and temporal changes in litter quality are possible. As the three isopods exhibit clear feeding preferences (Ma, 1988), their population sizes may have been affected by the availability of high- quality food. Investigations of this matter are continuing.

Influence of biological factors

Although predation may significantly influence isopod population size (Paris & Pitelka, 1962; Sutton, 1970; Sunderland, Hassall & Sutton, 1976; Sunderland & Sutton, 1980), our data did not allow a rigorous examination of this aspect. Cannibalism may be important in laboratory cultures of isopods (Sutton, 1980). and was noted in cultures of F. rufluelei, but its significance in nature is unclear. Victims of cannibalism were either moulting or infected by Rickettsiella (Rickettsiae), which reduced locomotory ability. Rickettsiella is a small, gram-negative, bacteria-like organism, commonly associated with insects and arachnids (Federici, 1984). In Hong Kong, F. ruflaelei and 0. maculatus were heavily infected by Rickettsiella (respectively, 22.3 and 20.8% of sampled

364 H. H. T. MA, D . DUDGEON AND P. K . S. LAM

individuals), which may have been due to their contagious distribution, cannibalism or carcass- feeding habit. It should be noted that, in the present study, the diagnosis of Rickettsiella infection was possible only in the advanced stages (1.e. white masses of infected connective tissue appeared in the isopod haemocoel), and thus, the observed infection rates must have been underestimated. The above findings suggest that the abundance of the two armadillids may be significantly affected by Rickettsiella.

Dipteran parasitoids have been thought to have an important influence on isopod populations (Sutton, 1980; Sassaman & Garthewaite, 1984). Although nematode parasites and dipteran parasitoids infect F. rufaelei in Hong Kong, the incidence was low ( c 0.1 %). However, the possible role of pathogens-specially Rickettsiella-and parasites in shaping the population dynamics of isopods clearly deserves and requires further investigation.

Professor P. Calow, Professor M. R. Warburg, Dr K. Wilson and an anonymous referee are thanked for their constructive comments on a version of the manuscript.

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