1. at the Porcupine Abyssal Plain, NE Atlantic.
Functional shifts in abyssal nematodes: a 15-year period study ( )
at the Porcupine Abyssal Plain, NE Atlantic.
Vasiliki Kalogeropoulou 1,2,3*, N. Lampadariou ¹, A.J. Gooday 4, P. Martinez Arbizu 2,3, A. Vanruesel 5
1Hellenic Centre for Marine Research, P.O. Box 2214, Heraklion, Crete, 71003, Greece
2 University of Oldenburg, Department of Biology, Oldenburg, 26129, Germany
3DZM3 German Centre for Marine Biodiversity Research, Senckenberg am Meer, 26382,Wilhelmshaven, Germany
4Ocean Biogeochemistry and Ecosystems Research Group; National Oceanography Centre, Southampton SO14 3ZH, UK.
5Universiteit Gent; Faculteit Wetenschappen; Vakgroep Biologie; Afdeling Mariene Biologie
Fig. 1. Charts showing (A) the general location of the Porcupine Abyssal Plain Sustained Observatory site PAP-SO, 48°50´N, 16°30´W) and (B) the disposition of samples assessed in the present study.
Introduction
Time series studies (>15 y) in abyssal benthic communities, conducted at the Porcupine Abyssal Plain in the NE
Atlantic, at 4850 m water depth (Fig. 1), since 1989, have revealed long-term changes in megafaunal communities,
possibly linked to climatic fluctuations that influence organic matter supply [1]. Observations at the PAP revealed a
strong seasonal deposition of phytodetritus during some years and a radical shift in megafaunal abundance and
community structure, notably a dramatic increase in densities of the holothurian Amperima rosea during ‘96-’04.This
so-called ‘Amperima Event’ [2] is believed to be related to changes in the quantity and quality of organic matter
reaching the seafloor [3]. A similar phenomenon, also possibly linked to climatic oscillations, was observed at the
Station M in the NE Pacific (34°50´N, 123°00´W) [4]. Smaller size classes of the benthic community, the meiofauna
[5], the foraminiferans [6] and the macrofauna [7], have also exhibited population changes over the course of the
PAP time series.
Nematodes, the dominant meiofaunal taxon at the PAP (’89-’04), exhibited
a 3-fold increase in abundance since 1996 (Fig.2) apparently influenced by the
upward trend in organic matter fluxes and the macro- and mega-faunal activity.
Correlations with fluxes, however, were weak and flux peaks did not coincide
with density peaks, indicating a time-lagged response [5]. The most abundant
species exhibited temporal variations and shifts in assemblage composition
That were due to the substitution of rare species between the “pre-Amperima” &“Amperima” periods. Unlike the
temporal trend in densities, nematode species richness decreased during the
Amperima period, shifting to a community defined mainly by opportunistic species. September ‘96 and March ‘97 was a
transitional period for the nematodes, unlike the larger size categories, particularly the megafauna, which exhibited
an immediate response[8].
In the present study the temporal variability in biomass and functional diversity were investigated taking into
account the size spectra and functional complexity of the nematode assemblages. Combining biomass data and a range
of biological traits based on buccal morphology, tail shape, body size, body shape and life history strategy, the
questions below were addressed: 1. Are there any temporal variations in nematode size and biomass triggered by the
changes observed in 1996? 2. Are there any temporal variations in nematode biological traits due to changes in
environmental conditions? 3. Do the community shifts observed in nematode assemblages exhibit a stronger signal
through a functional group approach?
Fig. 2. Temporal variability in nematode densities (Ind.*10cm²), particulate organic carbon flux (g*m-2*yr-1) and biomass (μgr).
Biological Traits
Low values of the trophic index indicated a
highly diverse community, when referring to
feeding strategies. Selective deposit feeders
increased with time due to the increased food
supply. Non-selective deposit feeders and
epigrowth feeders exhibited a significant
3-fold & 2-fold increase during the Amperima
period. Large predators were only marginally
present, due to the lack of freshly dead
organisms. The three feeding groups coexist
in large numbers since July ’97 indicating a variability in size, shape and quality of the available food and thus an efficient resource partitioning is accomplished amongst several nematode species with similar food preferences.
Tail shape group proportions were significantly variable providing ecological information not incorporated in
the rest of the biological trait groupings since particular tail shapes were not restricted to particular buccal morphologies. 50% of the species had elongated/filiform tails, being favoured during the Amperima period due to their locomotion capabilities.
Small and slender nematodes dominated the assemblages (82%) presenting a significant 2-fold increase
during the Amperima period. Although stout nematode densities were incomparable to the slender ones, their presence was functionally substantial to the assemblage in a long temporal scale. Long and large (>2mm) nematodes, which are known to inhabit usually the deeper sediment layers, were immediately influenced by the Amperima event as they increased significantly their low in general densities during the Transition period and decreased again from July ‘97 onwards, when small and slender nematodes took over.
Colonisers (c-p2) were substantially more abundant (40%), yet groups with intermediate characteristics
(c-p3) and persisters (c-p4) depicted high proportions to the total nematode assemblage as well (33% & 27%). The decreasing temporal trend in the Maturity index (MI) indicated an increasing microbial activity and a predominance of colonisers during the Amperima years. Assuming that prior to ‘96 the PAP was a stable habitat characterized by a range of species with narrow ecological niches, disturbance caused by the increased fluxes and the intense megabenthic activity influenced the most sensitive species the niches of which remained vacant or were filled gradually by less specialised species or species with a higher reproductive potential, resulting in a decreasing Maturity Index.
Table 1. Temporal trends in nematode density, size spectra, buccal morphology, tail shape, life history strategy, body shape, body length and functional indices at the PAP ( ). ANOVA results are shown for between periods (’91-’94 vs. ’96-’97 Mar vs. ‘97July-’04), years and cruises (time points) comparisons. (ns - not significant).
180 nematode species were pooled into 56 functional groups. The biological traits matrix (Fig. 5a) revealed the predominance of 5 functional groups which belong to 3 functional complexes exhibiting significant contribution to the observed temporal variability. The most dominant functional complex, plus the first to respond to the Amperima event, consisted of c-p3 epigrowth feeding slender chromadorids (Acantholaimus, Chromadorita, etc.), bearing 2 different locomotion strategies. The second functional complex consisted of c-p2 deposit feeding slender monhysterids (Thalassomonhystera, Theristus, etc.) and the last important functional complex consisted of c-p4 selective deposit feeding corpulent Desmoscolecoidea (Desmoscolex, Tricoma, etc.). The 2nd stage MDS (Fig. 5b) revealed a significant separate clustering between the functional groups densities matrix (BTM) and the single functional characteristics matrices (rs=0.58) as well as the taxonomical densities and biomass matrices (rs=0.65).
Fig. 5. a) nMDS ordination plot based on the presence/
absence Biological Traits Matrix and b) 2nd stage MDS ordination plot of inter-matrix rank correlations.
Nematode biomass and size spectra
Nematodes at the PAP were on average μm long, μm wide, with a
L:W ratio of 28, being consistent with the general tendency for small sized nematodes
at the deep sea areas worldwide. Total biomass was 40.2 μgr/10cm² and individual
biomass 0.36 μgr . Temporally, nematode length and width deviated from the average
(Fig.3) exhibiting a significant increase (L: μm;W: μm) during the
Transition period (September ‘96 & March ‘97), a year after the first significant
increase of downward fluxes coinciding, simultaneously, with the population explosion
of holothurians. During the Amperima period, from July ‘97 onwards, both length and
width (L: μm;W: μm) decreased significantly, resulting in an assemblage
where slender and small sized nematodes predominated.
Total biomass, on the other hand, exhibited an increasing trend ranging between
μgr/10cm2 with two substantial peaks in September ‘96 and October ’02.
A correlation between food availability and nematode size and biomass was revealed,
yet with a time delay between maximum food supply and maximum growth of the
nematodes, indicating a time lagged response of the nematode assemblages to the
increased input of POC fluxes.
Fig. 3. Temporal variation of nematode size spectra at the PAP ( ): average biomass displayed on X2 geometric weight classes (a); Average length (b) and length/width ratio on linear scale (c).
The small nematode size in the deep sea is optimal, and deviations only
occur when environmental conditions change. ABC curves (Fig. 4) revealed a
moderately disturbed nematode assemblage in September ‘96 and March
’97 which coincided with the population explosion of the holothurians. This
emphasized the significant biochemical changes of the benthic environment
at the specific time points and supported the proposed Transition period
that nematodes went through before responding to the increased
phytodetritus fluxes and going back to an undisturbed condition from July
‘97 onwards. The substantial impact of the stability or not of the sediment
biogeochemical conditions on the nematode size and taxonomic structure
could be an explanation of their different response to the deep-sea
environment compared to other benthic organisms.
Fig.4. Abundance/Biomass comparison method (ABC) plots detecting the undisturbed, moderately disturbed or disturbed condition of the nematode assemblages at the PAP ( ).
Conclusions
The temporal changes observed in the size spectrum of the nematode assemblages at the PAP supported the corresponding food availability related shifts in their species composition.
Significant biogeochemical changes took place in the benthic ecosystem at the PAP during ‘96 and March ’97 creating a moderately disturbed nematode assemblages and evoking community composition shifts. This was clearly a Transition period for the nematode communities.
All biological traits exhibited significant temporal variability indicating substantial functional shifts in the nematode assemblages in a long temporal scale.The biological traits matrix revealed the predominance of 3 functional trait combinations (functional group complexes) which were primarily responsible for the temporal variability observed.
The significant separate clustering of matrices based on functional, taxonomical and size spectra characteristics revealed that the information provided by a single functional characteristic is not a mere reflection of the information provided by another, increasing at the same time the importance of taxonomic, functional and morphometric information to an integrated community structure analysis.
The significance of several numerically less abundant species is revealed when they are incorporated, based on their biological trait characteristics, in functional groups which is totally overlooked in species diversity studies.
Following a functional approach gives us a more detailed insight of the structure of nematode assemblages and their ecological functions. Further knowledge of species physiology is needed for the efficient interpretation of the functional structure results in order to identify the missing links and comprehend their functional purpose and importance in the benthic ecosystem.
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