114 H
. Zhou J. Exp. Mar. Biol. Ecol. 256 2001 99 –121 Table 8
SIMPER analysis of the nematode community identifying the top three species making the biggest percentage contributions to Bray–Curtis dissimilarities based on single square root transformed abundance data
between treatments at a specific stage of the experiment. C, control; L, low dose; M, medium dose; H, high dose
Samples 10 Days
30 Days 60 Days
compared Species
Species Species
a a
a
C and L Diplolaimella sp.
15.6 Diplolaimella sp.
28.4 Diplolaimella sp.
21.8
a a
Theristus sp. 11.6
Chromaspirina sp. 5.2
Chromaspirina sp. 6.0
a a
Unidentified species 5.6
Haliplectus wheeleri 3.0
Desmodora cazca 4.4
a a
a
C and M Diplolaimella sp.
13.1 Diplolaimella sp.
18.6 Diplolaimella sp.
37.2
a a
a
Theristus sp. 7.6
Theristus sp. 10.0
Megadesmolaimus sp. 3.5
a
Unidentified species 5.6
Chromaspirina sp. 6.8
Diplolaimelloides sp. 2.9
a a
a
C and H Diplolaimella sp.
8.0 Diplolaimella sp.
23.5 Diplolaimella sp.
35.2
a a
Unidentified species 7.1
Diplolaimelloides sp. 5.5
Anoplostoma viviparum 4.4
a a
a
Diplolaimelloides sp. 6.7
Theristus sp. 5.5
Dichromadora sp. 3.3
a a
L and M Diplolaimella sp.
12.6 Diplolaimella sp.
13.7 Diplolaimella sp.
24.3
a
Theristus sp. 9.3
Theristus sp. 10.3
Chromaspirina sp. 5.3
a a
Diploliamelloides sp. 6.6
Chromaspirina sp. 5.8
Megadesmolaimus sp. 4.3
a
L and H Diplolaimella sp.
12.2 Diplolaimella sp.
16.2 Diplolaimella sp.
27.4
a a
Theristus sp. 10.8
Theristus sp. 7.2
Anoplostoma viviparum 4.7
a a
Diplolaimelloides sp. 8.8
Diplolaimelloides sp. 6.1
Chromaspirina sp. 3.9
a
M and H Diplolaimella sp.
12.1 Theristus sp.
11.1 Diplolaimella sp.
23.1
a a
Theristus sp. 7.3
Diplolaimella sp. 8.0
Anoplostoma viviparum 4.9
a a
Diplolaimellodies sp. 6.3
Chromaspirina sp. 5.9
Paracanthochus sp. 4.1
a
Average density of the species is higher in the latter sample.
field control and different levels of treatment if the two numerically dominant species, namely Parastomanema sp. and Diplolaimella sp., were not included Fig. 8A,B.
4. Discussion
Meiofaunal responses to leaf litter additions not only differed among different major taxa but also varied over decomposition time. The meiofaunal colonization of ex-
perimental sediments during earlier stages, i.e. days 1 to 10, indicated a negative effect of newly-added leaf litter on the colonization of total meiofauna, copepods and
polychaetes. This was possibly related to mangrove-derived tannins or other polyphenic acids. In five mangrove estuaries in Australia, nearly all of the dominant meiofaunal taxa
correlated negatively with concentrations of sediment tannins in the low- and mid- intertidal zones Alongi, 1987b. The field evidence of a negative effect of mangrove-
derived tannins on meiofauna was supported by a nematode growth experiment, in which the population growth of Terschellingia longicaudata was limited by Rhizophora
stylosa which contained the highest concentration of tannins of three potential food types Alongi, 1987b. Tong 1998 recorded high tannin concentrations in Kandelia candel
H . Zhou J. Exp. Mar. Biol. Ecol. 256 2001 99 –121
115
Fig. 7. Changes in nematode trophic composition over the experimental period. Numbers ind. per core are obtained by averaging replicates for each treatment at each sampling date. 1A, selective deposit feeder; 1B,
non-selective deposit feeder; 2A, epi-growth feeder; 2B, predator omnivore. To make the plots comparable, Diplolaimella sp. is not included due to its extremely high numbers. C, control; L, low dose; M, medium dose;
H, high dose.
leaves from Ting Kok mangrove 12.11 dry wt. for young leaves and 7.25 for mature leaves, and which were close to those of R. stylosa 11.45 for the fresh and
8.23 for 1 week aged leaves reported upon by Tietjen and Alongi 1990. However, nitrogen content was higher in K
. candel 1.86 for young leaves and 1.83 for mature leaves than in R. stylosa 1.04 for fresh and 1.28 for 1 week aged leaves. Litter bag
studies indicated that rapid 14–40 days loss of tannins from ready-to-fall, senescent
Fig. 8. A comparison of nematode trophic composition between field control F and treatments C, L, M and H at the end of the experiment 60 days. Parastomanema sp. Pa and Diplolaimella sp. Di are
included in A and not included in B. Other abbreviations as used in Fig. 7.
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mangrove leaves R. stylosa, Avicennia marina and Ceriops tagal can coincide with rapid increases in densities of bacteria on them Robertson, 1988. Community
development on the leaf litter could be affected and controlled by changes in leaf chemistry and the successional development of the microphyte community Gee and
Somerfield, 1997. Despite a high tannin concentration in K
. candel leaves, the also high nitrogen content may be of more importance for meiofaunal community development
during the later stages of colonization 30–60 days, as in this study. With an increasing decay time for leaf litter, negative effects shifted to positive ones. By the end of this
experiment 60 days post-placement, nematodes and the total meiofauna showed significantly positive responses to the addition of detritus in terms of their relative
numbers among the control and different levels of leaf litter addition. A positive response was less evident for copepods and polychaetes. In a north-eastern Malaysian
mangrove, Gee and Somerfield 1997 observed that changes in the copepod community on the leaf litter Rhizophora apiculata and Bruguiera parviflora were basically an
expression of the life cycle of Darcythompsonia. In the present study, the lower P value of 60 days Table 4, P 5 0.089 compared with 30 days post-placement Table 4,
P 5 0.251 indicated that a positive response by copepods to leaf litter may exist but could not be detected because of a lack of power in the experimental design few
replicates. Another explanation for this may exist if different colonization mechanisms by the meiofaunal taxa are taken into account. For a small-scale defaunation, nematode
dispersal occurs either via suspended or infaunal movement in a uniform way, whereas copepods recolonize sediments predominantly from the water column. The relatively
surficial distribution of copepods enhances the probability of passive suspension from current action and limits the possible pathways for infaunal movement Chandler and
Fleeger, 1983. During a vertical distribution study conducted in this mangrove, 53 of nematodes and 96 of copepods were found in the 0–2 cm depth. In this experiment,
therefore, leaf litter supplies in the experimental sediment column 0–8 cm in depth may not be fully available to copepods and, accordingly, their numbers may not be a
true reflection of treatment effects.
Nematode community succession was tightly linked to the leaf litter decomposition process in terms of density, species diversity, community structure and trophic
composition. Individual numbers increased but species numbers and dominance-based diversity indicated by the K-dominance curve decreased with an increased level of leaf
litter addition. Community structure and species composition differed among controls and detritus samples. All the differences associated with leaf litter addition could be
attributed to the occurrence and rapid increase of a small bacterivorous species, Diplolaimella sp., in the detritus-enriched samples. Many studies Lorenzen, 1969;
Hopper, 1970; Hopper et al., 1973; Alkemade et al., 1994 have suggested that detrital systems where either marsh vegetation or mangrove leaves predominate are dominated
by two closely related nematode genera, namely Diplolaimella and Diplolaimelloides. These genera of nematodes have been studied intensively in terms of their roles in the
detrital system Milton, 1981; Findlay and Tenore, 1982; Alkemade et al., 1992a,b and various studies indicate they are bacterial feeders Tietjen and Lee, 1977; Deutsch, 1978;
Moens and Vincx, 1997; Moens et al., 1999. On one hand, therefore, the population growth rate is expected to depend on the bacterial biomass production and, on the other
H . Zhou J. Exp. Mar. Biol. Ecol. 256 2001 99 –121
117
hand, their presence can stimulate bacterial growth and thus, in turn, enhance the rate of organic detritus breakdown Warwick, 1987.
Diplolaimella sp., even though dominant in all the detritus samples, was rare in the ambient mangrove sediment in the study site. In a colonization experiment of PCP-
contaminated sand, Cantelmo and Rao 1978 found the abundances of Diplolaimella punicea in high and medium dose treatments were significantly higher than the control
and low dose ones. Initial colonizers, after defaunation caused by physical disturbances, are normally opportunistic species, which are well adapted to the niches hence made
available to them and are able to utilize the newly available resources quicker than their competitors Grassle and Grassle, 1974. As an opportunistic species, Diplolaimella sp.
has an r-strategy life history that is characterized by a relative short generation time, a high reproductive potential and rapid rate of population growth Warwick, 1987.
Moreover, Diplolaimella sp. can take advantage of the food available, i.e. bacteria, which are the first colonizers and can grow rapidly during decomposition of the organic
resource leaf litter or even PCP. In laboratory microcosms, in the absence of meiofauna, colonization of debris derived from algal and salt-marsh plants is succession-
al, with bacteria followed by flagellates and ciliates Newell, 1982.
Diplolaimella sp. was highly dominant numerically in the detritus samples, and thus dose effect on the successional development of nematode species assemblage could be
controlled by this species. Lack of evidence of strong dose effect between M and H dose regimes in particular on the population growth of Diplolaimella sp. and,
accordingly, nematode diversity, community structure and trophic composition may be because of the limited space and exchange using the tubes for a full development of the
Diplolaimella sp. population proportional to the high food quantity. But no attempt was made to evaluate procedural effects.
The generation time of Diplolaimella ocellata, a species associated with mangrove leaves, is only 5–7 days at 308C Hopper et al., 1973. In a temperate salt marsh,
Alkemade et al. 1993 showed that the number of Diplolaimella dievengatensis was most related to the decomposition rate of Spartina anglica leaves in spring, summer and
autumn, but not in winter. At the study site in summer, when this experiment took place, the average sediment temperature was 328C. At this temperature, population growths of
bacteria and Diplolaimella sp. could be rapid in the detritus samples, but the same colonization pattern may not take place if the experiment was conducted in winter.
The differentiation in nematode community structure and trophic composition between experimental samples and natural environment and between various levels of
detritus enrichment was basically an expression of relative abundance of Paras- tomanema sp. and Diplolaimella sp. in different samples and most possibly a reflection
of their different sources of nourishment, crawling abilities and life histories. Paras- tomanema sp., a mouthless species, has a large body length width ratio a 5 120 and a
deeper distribution .2 cm in depth. Its high dominance 40 of total nematode density indicated low oxygen tension in the mangrove sediment as well as its successful
adaptation to this harsh environment by means of epidermal uptake of dissolved organic matter Jensen, 1987b.
Besides the overwhelming dominance of Diplolaimella sp. in the detritus samples, other species such as Diplolaimelloides sp., Theristus sp., Megadesmolaimus sp.,
118 H
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Anoplostoma viviparum and Haliplectus wheeleri were also more abundant than in the controls. These species are all deposit feeders Types 1B and 1A in Wieser’s trophic
group scheme. These results are in agreement with those of previous studies in terms of species and trophic composition, though the colonization time scale related to the
decaying leaf litter was not well comparable because of the different methods employed. In a temperate salt marsh, Alkemade et al. 1993 demonstrated that the numbers of
some deposit-feeding species, namely Diplolaimella dievengatensis, Diplolaimelloides bruciei, Theristus acer, Desmolaimus zeelandicus and Monhystera parva, were positive-
ly correlated with decomposition rates of Spartina anglica leaves. Similarly, Gee and Somerfield 1997 showed that the majority of nematode species colonizing mangrove
leaves are bacterial and deposit feeders like Perspiria sp., Theristus sp. and Diplolaimel- loides sp., etc. The fact that some epi-growth feeders, such as Desmodora cazca and
Dichromadora sp., also responded positively to leaf litter additions and all the trophic groups reached highest numbers in the high dose treatment by the end of the experiment
indicated a successional order of nematode trophic groups over the leaf litter decomposi- tion process. This study suggests that deposit-feeding nematodes, especially bacterial
feeders, are pioneer colonizers of the leaf litter and may play an important role linking detritus and decomposer to higher trophic levels. Nevertheless, lack of spatial replication
in the experimental design could limit the generality of the findings and, thus, complementary field and or laboratory studies are still needed.
5. Conclusions
