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Colonization of soft sediments by benthic communities: An experimental approach in Admiralty Bay, King George Island
Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
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Colonization of soft sediments by benthic communities: An experimental approach in Admiralty Bay, King George Island Yargos Kern a,⁎, André Rosch Rodrigues b, Theresinha Monteiro Absher a a b
Universidade Federal do Paraná, Centro de Estudo do Mar, Laboratório de Moluscos Marinhos, Av. Beira Mar s/n, 83255–976 Pontal do Paraná, PR, Brazil Universidade de São Paulo, Instituto Oceanográfico, Departamento de Oceanografia Biológica, 05508–900 São Paulo, SP, Brazil
a r t i c l e
i n f o
Article history: Received 30 September 2013 Received in revised form 20 December 2013 Accepted 23 December 2013 Available online 19 January 2014 Keywords: Antarctica Colonization Macrobenthos Soft-sediment
a b s t r a c t In order to understand nearshore biological community colonization following impact events that affect the distribution and occurrence of species and subsequent recovery a manipulative experiment was set up in King George Island. This work aimed to study colonization patterns of benthic macrofauna in defaunated soft sediment, comparing them with occurrence patterns of macrofaunal benthic organisms found in the natural soft sediment of adjacent areas, in shallow waters of Admiralty Bay, King George Island, Antarctic Peninsula. For this, a manipulative field experiment was installed through SCUBA diving at 22 m depth in front of the Antarctic Brazilian Station. Samples of defaunated and natural soft-sediments were analyzed. Defaunated soft sediment in plastic boxes (a = 0.02 m2) were deployed in the seabed and examined after 6, 12 or 18 months. Natural soft-sediment collected with cylindrical corers of 10 cm in diameter (a = 0.08 m2), in adjacent areas at the experiment installation and during the changing and removal of the experimental boxes, were also analyzed. Altogether, 20,680 organisms belonging to 6 phyla among 42 species were identified. Thirty three taxa out of the 42 recorded were common in both natural and defaunated sediment types, 6 taxa occurred only in natural sediment and 3 taxa only in defaunated sediment. The most abundant groups throughout the experiment were: Oligochaeta, Polychaeta, Bivalvia, Gastropoda and Crustacea. In the natural sediment a total of 10 species were considered Constant, 8 species Accessory, 21 species Accidental. In the defaunated sediment 14 species were Constant, 4 species Accessory, 18 species Accidental. Analysis of variance indicated significant differences in total abundance and in Torodrilus sp. abundance in the periods of 6 and 18 months, and MDS analysis showed a clear separation between natural and defaunated treatments. Torodilus sp. was the taxon with the highest relative contribution (26%) in natural sediment. In the defaunated sediment treatments, the most common taxa were cumacean Leuconidae morphotype 1 (19%) and the bivalve Yoldia eightsi (Couthouy, 1839) (18%). The statistical results indicated significant differences between the natural and defaunated treatments with respect to benthic macrofaunal associations. Species richness and abundance in defaunated treatment were less than in natural treatment. The results suggest that recovery levels in Antarctic waters after events of defaunation are very low and in order to be of value experiments may need to be for longer periods. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Recruitment to the substratum is a crucial event in the life cycle of benthic marine invertebrates when organisms are changing in habitat and life style by settlement and early development (Stanwell-Smith and Barnes, 1997). Studies of benthic species generally consider that new settlers can arrive at a place by two main ways: 1) recruitment of pelagic larvae; 2) migration of juvenile and adults from nearby areas (Smith and Brumsickle, 1989). The life cycle of benthic species can include the indirect development with planktonic larvae (planktotrophic or lecithotrophic), the direct development with incubation of embryos and hatching of ⁎ Corresponding author. Tel.: +55 4291024673. E-mail address: [email protected] (Y. Kern). 0022-0981/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jembe.2013.12.019
juveniles' forms, or mixed development, of various incubation degrees and hatching stage of larvae (Absher et al., 2003; Barnes et al., 1993; Giese and Pearse, 1977; Hoffman et al., 2013; Peck, et al., 2006). Larval-stage duration depends on many related factors, for instance, egg type and food availability and physical-chemical conditions of seawater. Metamorphosis may happen before, during or after settlement, and in all cases the larvae becomes negatively phototactic and/or positively geotactic and goes to the sea bottom. The larva tests the physical, chemical and biological conditions of the substratum and when finding a suitable situation, completes its metamorphosis (Brusca and Brusca, 1990). Larvae are present in the water column all year round in Antarctica (Bowden et al., 2009) and settlement of some groups occurs over different periods (Pearse et al., 1991, Bowden et al., 2006). In Admiralty bay, with the beginning of the austral summer (November to March),
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Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
Fig. 1. EACF location in Martel Inlet (modified from Simões et al., 2004).
begins the supply of larvae or juveniles from the water column or sediment from adjacent areas (Freire et al., 2006). The success of larval recruitment may be affected by several factors, including the presence of adults, the hydrodynamic properties of the area, the existence of chemical traces, or some combination of these factors. While larval supply may
Table 1 Dates of installation, retrieval, time of permanency and boxes numbers of the colonization experiment in defaunated sediment. Installation
Retrieval
Permanency
Area
Box no.
December 2002 December 2003 December 2002
December 2003 June 2004 June 2004
12 months 6 months 18 months
I–III Ib–IIIb II–IV
1 to 4–9 to 12 1b/4b–9b/12b 5 to 8–13 to 16
be limiting or not, the success in the species colonization depends on the nature of the existing community together with the attributes of the local substratum, as, for instance, its stability (Constable, 1999). Processes that govern the survival and dispersion of planktonic larvae in the water column are very different from the mechanisms of substratum selection, metamorphosis and settlement of larvae, with transitional behavior occurring between planktonic and benthic stages. Substratum colonization during this period is complex, with dominance patterns and composition of the benthic community changing through time (Bromberg et al., 2000; Nonato et al., 1992). The importance of studies coupling the distribution of established taxa and substratum colonization in ecology of benthic invertebrates has been recognized since the adults' populations are linked by the dispersion of the larval stages (Bostford et al., 1994).
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
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Table 2 Dates of natural sediment removal, period, experimental area and corer numbers.
Fig. 2. Chronological sequence of the periods of placement and retrieval of the plastic boxes for the colonization experiments of defaunated soft sediment.
The absence of a biologically relevant bathymetric variation in temperature allows a majority of Antarctic benthic species to occupy a very wide distributional pattern. Several species, whose occurrence is characteristic of shallow waters elsewhere, can extend to 500 to 1000 m of depth (Arntz et al., 1994). Moreover, in the shallow coastal zone distributions are more complex, not only exhibiting vertical zonation (Bromberg et al., 2000), but also a complex patchy distribution pattern (Bromberg et al., 2000; Nonato et al., 2000). Shallow-water colonization patterns in Admiralty Bay are especially influenced by the mechanical effect of ice. This can include the freezing of the intertidal area, as well as the impact of icebergs, evidenced by scars, disturbing or even removing benthic organisms, creating a community mosaic with different stages of succession (Dayton et al., 1974). Natural communities form those mosaics and they tend to vary unpredictably in time and space. That variability can be measured by changes or differences in the abundance of species, or in the diversity of the association (Underwood et al., 2000). Iceberg scour has been described as a major source of disruption of Antarctic near shore marine communities (Barnes and Clarke, 1994; Peck and Bullough, 1993; Rauschert, 1991). Benthic, shallow-water communities are composed by organisms of long life (Arntz et al., 1994; Clarke, 1996) and their recovery from ice impacts may take years (Arntz et al., 1994). To understand the significance of disturbance events and of benthic macrofaunal patterns of colonization requires carefully constructed colonization experiments, but such experiments are practically nonexistent in the Antarctic coastal
Date
Period
Area
Corers no.
December 2002 December 2003 December 2003 June 2004 June 2004 June 2004 June 2004
Initial (T0) 12 months (T12) 12 months (T12) 6 months (T6) 6 months (T6) 18 months (T18) 18 months (T18)
I, II, III, IV I III I III II IV
8 in each area 8 8 8 8 8 8
ecosystems (Arntz et al., 1994). The few previous studies reported (Barnes, 1996; Dayton, 1989; Rauschert, 1991) have suggested that recruitment levels in Antarctic waters are very low and that to be of value, settlement experiments may need to be immersed for extended periods. Assessing colonization patterns of the benthic macrofauna in Admiralty Bay is one of the first steps to determine the factors that contribute to or disturb the resilience and persistence of those communities. The differences observed in the communities of Antarctic shallow waters over time depend on when the disturbance occurred, relative to the availability of larvae and juveniles for colonization (Nonato et al., 2000). If the availability of larvae and juveniles varies during the austral summer, communities in which the composition and dominance are different may result, creating a faunistic mosaic in the shallow coastal zone. Slow growth, maturation and great longevity are characteristics of the Antarctic benthic macrofauna that are influential in the colonization dynamic (Arntz et al., 1994). Colonization by benthic macrofauna in experimental panels or in hard substrata has been performed in recent years in Antarctica (Barnes and Conlan, 2007 for review). However, manipulative experiments for the study of soft sediment colonization by macrobenthic fauna are a rare practice in Antarctic shallow waters. In the Arctic environment Veit-Köhler et al. (2008) studied meiobenthic colonization in soft-sediments in Kongsfjorden (Svalbard). Data obtained by this type of research permits the evaluation of the communities' recovery capacity as well as the efficiency of the species dispersion processes. This study is a first step to determine factors that contribute to or disturb the resilience and persistence of soft-sediment benthic communities in Antarctic shallow coastal waters. A manipulative field experiment was used to assess whether benthic invertebrate fauna colonized defaunated sediment at the same temporal pattern as natural sediment. The experiment allowed the evaluation of colonization pattern and community structure after 6, 12 and 18 months of a field experiment as an indication of recovery in the event of iceberg scouring in the area. The goals of our study were to determine temporal patterns of colonization of marine benthic fauna in experimentally defaunated soft sediments and to compare those with patterns of occurrence of benthic fauna in natural soft sediments from adjacent areas. The aim was to test the hypothesis that there will be differences in the composition of the benthos between the natural and defaunated soft sediment. 2. Material and methods 2.1. Study area
Fig. 3. Schematic placement of the boxes with defaunated sediment and areas of natural sediment sampling with corers.
Martel Inlet (Fig. 1), where the Brazilian Antarctic Station “Comandante Ferraz” (EACF) (62°05′S–58°23′W) is located, has a maximum depth of about 250 m. The bottom topography in front of the station includes a steep slope down to 30 m, with multiple deep scours and troughs from ice action at a depth around 18 m. In general, the sediments include gravely sand at 6 m, becoming muddy sand at 30 m (Nonato et al., 2000). At about 22 to 25 m, a plateau is formed by medium silt (Bromberg et al., 2000). This area, apparently less subject to the impact of blocks of ice, presents a muddy bottom with an abundant sessile fauna (Nonato et al., 2000). This nearshore zone
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Table 3 Constancy index of taxonomic groups in natural and defaunated sediment. Taxonomic groups
Constancy index in natural sediment
Constancy index in defaunated sediment
Torodrilus sp. Dorvilleidae morphotype 1 Cirriformia sp. Diplocirrus sp. Haploscoloplos sp. Leitoscoloplos sp. Ophelina sp. Apistobranchus glacierae Hartman, 1978 Rhodine sp. Maldanidae morphotype 2 Levinsenia gracilis (Tauber, 1879) Capitella perarmata (Gravier, 1911) Erinaceusyllis cryptica Ben-Eliahu, 1977 Spirorbis nodenskjoldi Ehlers, 1900 Yoldia eightsi (Couthouy,1839) Thyasira falklandica (E.A.Smith,1885) Philobrya sublaevis (Pelseneer,1903) Mysella miniuscula (Pfeffer, 1886) Thracia meridionalis E.A.Smith,1885 Laternula elliptica (King & Broderip 1831) Onoba turqueti Lamy,1905 Laevilitorina antarctica (Smith, 1902) Nacella concinna (Strebel, 1908) Amauropsis rossiana Smith, 1907 Margarites refulgens (Smith,1907) Leuconidae morphotype 1 Cheirimedon femoratus (Pfeffer 1888) Gammaropsis georgianus Schellengerg, 1926 Uristes georgianus Schellengerg, 1931 Heterophoxus videns Barnard, 1930 Oradarea Walker, 1903 Oedocerotidae morphotype 1 Serolis polita (Pfeffer, 1887) Serolidae morphotype 2 Echinozone aries (Vanhoffen, 1914) Pseudocythereis spinifera Skogsberg, 1928 Doloria isaaczi Kornicker, 1971 Ctenocidaris speciosa Mortensen,1910 Ophionotus victoriae Bell, 1902 Parborlasia corrugatus (McIntosh,1876) Amphiporus lecointei (Bürger,1904) Priapulus tuberculatospinotus Baird,1868
Constant Accessory Constant Accidental Accidental Accidental Accessory Accessory Accessory Accidental Accidental – Accidental Accidental Constant Constant Accidental Constant Accidental Accidental Constant Accessory Accidental Accidental – Constant Constant Constant Accessory Accidental Accidental Accidental Accidental – Accidental Accessory Accidental Accidental Accessory Accidental Accidental Constant
Constant Accidental Constant Accidental Accidental Accidental Constant Constant Accidental Accidental – Accidental Accidental Accidental Constant Constant – Constant Accidental Accidental Constant – Accidental Constant Accidental Constant Constant Accessory Constant Constant Accessory Accidental Accidental Accidental – Constant Accessory – Accidental Accidental – Accessory
of Martel Inlet at 22 m depth was the site selected for an experiment to assess the benthic macrofauna colonization.
2.2. Experimental protocol During the XXI OPERANTAR (summer 2002/2003) the experiment was deployed by SCUBA divers in front of the Brazilian Antarctic Station (62°05′11.5″S–58°23′32.9″W). The sediment to be used in the experiment was collected at 22 m in an adjacent area using a van Veen grab. After defaunation by microwave under maximum power for 30 minutes, this sediment was examined and all animals remains Table 4 Occurrence of taxonomic groups only in natural or defaunated sediment. Taxonomic group
Natural (6)
Levinsenia gracilis (Tauber, 1879) Capitella perarmata (Gravier, 1911) Philobrya sublaevis (Pelseneer,1903) Laevilitorina antarctica (Smith, 1902) Margarites refulgens (Smith,1907) Serolidae morphotype 2 Echinozone aries (Vanhoffen, 1914) Ctenocidaris speciosa Mortensen,1910 Amphiporus lecointei (Bürger,1904)
Accidental
Defaunated (3) Accidental
Accidental Accessory Accidental Accidental Accidental Accidental Accidental
removed (including dead shells), sieved through 200 μm mesh and them distributed into 16 plastic boxes (0.17x0.12x0.10 m dimensions, with volume of 0.002 m3) and covered until placement on the sea floor (T0).The borders of the plastic boxes were set about 1 cm above the surface of the local sediment. Sediment analysis indicated the presence of silt sand sediments with poor organic matter content (5.00%) in the area of installation of the experiment. The overall area of the experiment was 9 square meters. The installation of the boxes, their removal, replacement and respective placement periods in the seabed, are indicated in Table 1. The chronological sequence of the periods and areas of settlement of the boxes are indicated in the Fig. 2. These boxes, according to their numbers and positioning, stayed buried in the sediment for periods of 6 (T6), 12 (T12) and 18 (T18) months. At the end of each period the boxes were removed by SCUBA divers, covered with a plastic lid underwater and transported to the EACF laboratory. Sediment samples were sieved through 200 μm mesh and preserved in 4% buffered formaldehyde. Organisms in the samples were sorted to the lowest possible taxonomic level (no dead shells were counted). The Fig. 3 illustrates the schematic positioning of the experiment, including the location of the plastic boxes in the sampling areas (area I, II, III and IV). Natural sediment samples taken outside the area of the boxes were collected with a cylindrical corer of 10 cm diameter buried 10 cm in the sediment. Eight replicates at each site, totaling 32 samples per
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
5
800
N 700
indivíduals / 0,1m2
D 600 500 400 300 200 100 0 I
II
III
IV
T0
I
III T6
I
III T12
II
IV T18
Fig. 4. Average and standard deviation of the number of individuals/0.1 m2, where: N = natural sediment, D = defaunated sediment; period T0 = initial, T6 = 6 months, T12 = 12 months and T18 = 18 months; and respective sampling areas.
period (T0, T6, T12, and T18) were taken. Core samples were processed using the same methods described above for the experimental treatments (Table 2). The surface area of one box (0.02 m2) corresponds, approximately, to the surface area of 2 corers (0.016 m2), and consequently, the surface area of the 4 boxes of an area (0.08 m2) corresponds to the surface areas of 8 corers (0.064 m2). 2.3. Data analyses The specimens were counted and identified to the lowest possible taxonomic level based on morphological characters and specialized literature (Absher and Feijó, 1998; Sieg and Wägele, 1990). Polychaetes were identified by Prof Dr Edmundo Ferraz Nonato of Instituto Oceanográfico (Universidade de São Paulo) and Dr Verônica Maria de Oliveira (Curso de Pós-Graduação em Zoologia, Universidade Federal do Paraná), crustaceans by Prof Dr Maria Teresa Valério Bernardo and Carina Waitman Rodrigues from Centro de Estudos do Mar (Universidade Federal do Paraná). Those data were then used to calculate the number of taxa, species richness (S), relative abundances (N) and Shannon diversity index (H′). For density, a matrix with the mean number of individuals from the replicates of all samples and respective treatments was organized. The quantitative results were then transformed in densities of individuals per 0.1 m2, according with the following: 2
D ¼ n x 0:1m =A where D = density, n = mean number of individuals per sample and A = total surface area of corers (0.064 m2) or boxes (0.08 m2) of a sampling area. The classification of Bödenheimer (1955) was used to determine the Constancy Index of species, relating the number of individuals of a species to the total number of samples. The following expression was used: Ci ¼ Si =nð100Þ where Ci = Constancy Index for species i, Si = number of samples with species i, n = total number of samples. This Index identifies the species as Constant when the percentage of occurrence is ≥50%; as an Accessory species when the occurrence percentage lies between 25 and 50%; and Accidental species, when the percentage of occurrence is ≤25%. For parametric statistical analyses, matrices of abundances of the species for each period (T6, T12 and T18), for treatment/period/area were built based on the standardization of the data in individuals/ 0.1 m2. The significance level adopted was α = 0.05 for all the tests.
The possible differences among biological variables in the natural and defaunated treatments were compared through ANOVA blocks design (Underwood, 1997), adopting the treatments (natural initial, final and defaunated) and periods (T6, T12 and T18) of sampling as fixed factors. The test a posteriori LSD (Least Significant Difference) was chosen for the comparison of the averages and was applied to all values of p. Prior to ANOVA, Levene's test was employed to test the homogeneity of variances and log (x + 1) transformation of the data was applied in cases of heterogeneity. Matrices were constructed using the Bray–Curtis similarity measure on log (x + 1) to normalize organisms' counts. Species-abundance data were calculated for samples and subjected to Q-mode cluster analysis to define assemblages. The Bray–Curtis distance was used to measure proximity between samples, and Ward's linkage method was used to arrange samples into a hierarchical dendrogram. The biological data were coordinated by non-metric multidimensional scaling (NMDS) (Dufrêne and Legendre, 1997) to emphasize the geometrical aspects of similarity and to enable visualization of complex data in a graphical environment. This approach highlights patterns that might not be apparent in cluster analysis and results in a map in which the placement of samples reflects the similarity of their biological communities and environmental patterns rather than their geographical location. The NMDS efficiency is demonstrated by the stress, that represents the necessary adjustment to represent the community in few dimensions (stress ≤ 0.2 = good ordination). The analysis of Similarity Percentage (SIMPER) was used to arrange into a hierarchy the species that contributed most to the similarity among the groups. 3. Results 3.1. Fauna A total of 20,680 individuals belonging to 42 taxonomic groups and 6 phyla were identified (Appendix A). Species of Oligochaeta, Polychaeta, Bivalvia, Gastropoda and Crustacea were the most abundant (Table 3). Thirty three taxa out of the 42 recorded were common in both natural and defaunated sediment types, 6 taxa occurred only in natural sediment and 3 taxa only in defaunated sediment (Table 4). In the natural sediment a total of 10 species were considered Constant, 8 species Accessory, 21 species Accidental. In the defaunated sediment 14 species were Constant, 4 species Accessory, 18 species Accidental. Torodrilus sp. of the Phylum Annelida, class Oligochaeta was the most frequent in all the treatments, and was a Constant species on both natural and defaunated sediments. Of thirteen identified
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Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
Fig. 5. Abundance of the groups in natural sediment in the initial period (T0).
Polychaeta species in 11 families, only Cirriformia sp. was Constant in the two sediment types, 2 species (Ophelina sp. and Apistobranchus glacierae Hartman, 1978) were Constant in natural sediment, and the remaining ones were considered Accessory or Accidentals. In Phylum Mollusca, both bivalves and gastropods were recorded. In the Class Bivalvia, 4267 individuals occurred from 4 families and 7 species. Yoldia eightsi was the more abundant (2409 individuals) species, followed by Mysella miniuscula (Pfeffer, 1886) (1454 individuals) and Tyasira falklandica (Smith, 1885) (358 individuals). Those three species were considered Constant in both sediment types. In the Class Gastropoda, 5 families were represented by a total of 804 individuals. Onoba turqueti Lamy,1905 was the only Constant species in the 2 sediment types, Amauropsis rossiana Smith, 1907 was Constant in natural sediment and the remaining species were considered Accessory, Accidental or absent. Among the crustaceans, the Amphipoda were most abundant, with 3684 individuals in 6 families with one species each. Cheirimedon femoratus (Pfeffer 1888) and Leuconidae (morphotype 1) were the only Constant species in the two sediment types, Gammaropsis georgianus Schellengerg, 1926 was Constant in natural sediment and Uristes georgianus Schellengerg, 1931 was Constant in defaunated sediment. In the order Isopoda, only 46 individuals in 3 families were represented by Accessory or Accidental species. The Class Ostracoda was represented by 311 individuals. The family Hemicyteridae (266 individuals) and
only one species, Pseudocythereis spinifera Skogsberg, 1928, was Constant in defaunated sediment. The family Cypridinidae (45 individuals) was represented by the species Doloria isaaczi Kornicker, 1971. The other groups, such as the Echinodermata, Nemertinea and Priapulida, were relatively rare. The specie Ctenocidaris speciosa Mortensen, 1910 (Echinodermata) occurred only once and the ophiuroid Ophionotus victoriae Bell, 1902 had a frequency of 115 individuals and was an Accessory specie in natural sediment and Accidental in defaunated sediment. The individuals from the Phylum Nemertea represented the families Lineidae, with the species Parborlasia corrugatus (McIntosh,1876) with 24 individuals, and Amphiporidae, with the species Amphiporus lecointei (Burger, 1904) with 4 individuals. The Phylum Priapulida had a total frequency of 75 individuals, all of the same species, Priapulus tuberculatospinotus, Baird, 1868, which considered Constant in natural sediment and Accessory in defaunated sediment. 3.2. Density and abundance Species with higher mean relative frequencies in natural sediment were: Oligochaeta Torodrilus sp (47.7%), Cumacea Leconidae morphotypy 1 (12.8%), Bivalvia Yoldia eightsi (12.0%). In defaunated sediment species with higher relative abundance were after 6 months: Amphipoda Cheirimedon femoratus (24.4%), Cumacea Leuconidae morphotype 1 (20.2%), Bivalvia Mysella miniuscula (14.4%) and Yoldia eightsi (12.6%)
Fig. 6. Abundance of Annelida, Mollusca and Crustacea in natural and defaunated sediment per periods and areas; N — natural, D — defaunated; period T6 — 6 months; T12 — 12 months; T18 — 18 months.
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
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Table 5 Summary of ANOVA and test a posteriori (LSD), considering as factor the period and treatment (i = natural initial, f = natural final, d = defaunated) and as variables the community's structural parameters (abundance, richness, diversity). T6 = period of 6 months, T12 = period of 12 months and T18 = period of 18 months. T6
Abundance Error LSD test Richness Error LSD test Diversity Error LSD test
T12
T18
MS
F
p
MS
F
p
MS
F
p
320,862 98,140
3.269
0.0496
176,392 191,593
0.921
0.4074
136,660 49,053
2.786
0.0767
(f N d) = i 1.638
0.2086
fNd=i 4.167
0.0236
(f N d) = i 3.183
0.0548
fNd=i 0.886
0.4209
2.225
0.1227
(f N d) = i 1.462
0.2469
27.169 16.589 0.17670 0.19934
53.344 12.800 0.48018 0.21582
fNd=i
51.821 16.278 0.22287 0.15249
(f N d) = i
and Gastropoda Amauropsis rossiana (10.1%); after 12 months: Amphipoda Cheirimedon femoratus (47.1%), Cumacea Leuconidae morphotype 1 (21.6%) and Bivalvia Yoldia eightsi (13.4%); after 18 months: Cumacea Leuconidae morphotype 1 (34.2%), Bivalvia Yoldia eightsi (23.4%) and Amphipoda Oedoceratidae morphotype 1 (19.4%) The highest mean densities were found: a) in NT0III in the period of the experiment installation (478.7 inds/0.1 m2), b) at 6 and 12 months in defaunated sediment in samples DT6I and DT12I (453 and 460 inds/ 0.1 m2, respectively, and at 18 months in natural sediment, sample NT18IV (460 inds/0.1 m2) (Fig. 4). Mean densities in natural sediment at 6 and 12 months were similar, except for area III, that showed a variation between 415 inds/0.1 m2 (NT6III) and 220 inds/0.1 m2 (NT12III). In defaunated sediment, the density values also were similar in the two sampling periods. At 18 months, the mean density of the natural sediment macrofauna of area II showed a significant low value (139 inds/0.1 m2), when compared to the other periods. Period of 6 and 12 months of defaunated sediment showed a smaller mean values of density in area III (245 inds/o.1 m2) when compared to area I, and a similarity in area IV (208 inds/0.1 m2) with area II. Abundance of the groups in natural sediment in the initial period (NT0) of the experiment are shown in Fig. 5 and subsequent abundance of the more representative taxonomic groups Annelida, Mollusca and Crustacea are in Fig. 6. Annellida were more abundant in natural sediment in all periods. Mollusks tended to be similarly abundant in the two types of sediment. Crustaceans presented the maximum abundance value (1188 individuals) in defaunated sediment in period DT12. Echinodermata, Nemertea and Priapulida were uncommon in all samples with the exception of Echinodermata (Ophionotus victoriae — 63 individuals) in natural sediment in the period NT18. 3.3. Analysis of variance The results of the evaluation of the community's structural parameters – abundance, species richness and diversity of Shannon –
fNd=i
are presented in Table 5. Data for the most abundant organisms of the taxonomic groups Annelida, Mollusca and Crustacea (the species Torodrilus sp., Y. eightsi and Leuconidae morphotype 1 respectively) are reported in Table 6. Analysis of variance revealed significant differences in the total abundance between final natural sediment and defaunated after 06 and 18 months. This difference was the consequence of the difference in the abundance of Torodrilus sp. (dominant species of natural sediment) in these periods. Significant differences were also observed in species richness at 12 and 18 months, in diversity and in abundance of Torodrilus sp. at 12 months and Leuconidae morphotype 1 at 6 months.
3.4. Cluster groups and non-metric analysis The Q Mode cluster analysis based on the overall species and ecological indexes revealed two groups and five subgroups (Fig. 7A and B). Group 1 is composed mainly by the defaunated samples; two subgroups can be distinguished, G1-A with DT18II, DT6IIIb, DT12III and DT18IV; and G1-B with the samples DT12I and, NT0IV. Some samples of natural sediment of this area and period were lost (and were not accounted for in the estimates) that may explain the low values of abundance (see Fig. 5). Group 2 is composed of natural sediment samples with three distinct subgroups. Subgroup G2-A with the samples NT6III, NT6I and NT18IV, G2-B with the samples NT12I, NT12III, NT0II and NT0III, and G2-C with the samples NT18II and NT0I. The sample DT6Ib did not belong to any group. The NMDS analyses performed using the biological data within collected samples showed the same groups as revealed in the cluster analysis (Figs. 7C and 8). Group 1 showed the lowest abundance of specimens and high values of Shannon diversity, especially in the subgroup G1-B. Amphipoda were abundant in samples in subgroup G1-A. Group 2 showed the highest abundance, especially in the subgroup G2-A, which has a high abundance of Annelida specimens (mainly Torodrilus.sp). Isopoda were abundant in the subgroup G2-B and the subgroup G2-C showed a high abundance of Echinodermata.
Table 6 Summary of ANOVA and test a posteriori LSD, considering as factor the period and treatment (i = natural initial, f = natural final, d = defaunated) and as variables the most abundant taxa (Torodrilus sp., Yoldia eightsi, Leuconidae morphotype 1). T6 = period of 6 months, T12 = period of 12 months and T18 = period of 18 months. T6
Torodrilus sp. Error LSD test Yoldia eightsi Error LSD test Leuconidae Error LSD test
T12
T18
MS
F
p
MS
F
p
MS
F
p
229,656.7 45195.7 (f N d) = i 4031.99 1860.22 f=d=i 20,472.7 5339.5
5.08139
0.011381
2.269
0.1180
0.0300
0.129174
1.889
0.1660
0.404
0.6707
3.83423
0.030933
0.124
0.8841
89,354.4 22787.4 (f N d) = i 673.53 1665.28 f=d=i 4552.6 3882.9
3.921
2.16748
282,843 124,651 (d b i) = f 3840.73 2033.58 f=d=i 335.60 2715.32
1.172
0.3225
(i = d) b f
f=d=i
f=d=i
8
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
(natural or defaunated). Torodrilus sp. was the dominant taxon in the natural sediment, with a relative contribution of 26%, and the crustacean Leuconidae morphotype 1, with a relative contribution of 19%, was the dominant in the defaunated sediment (Table 7). 4. Discussion
Fig. 7. Location of the boxes with natural and defaunated sediment in areas I, II, III, IV (A) and dendrogram classification (Q-mode) from abundance of species by areas and boxes (B) and NMDS of species occurrence by groups (C).
The relative contribution of the species, calculated by SIMPER analysis, among treatments and time, evaluated changes in the patterns of dominance of the macrofauna population for each sediment type
Results of the fauna composition showed 10 species to be constant representing 90% (18,640 individuals) from the total of 20,680 organisms belonging to the taxonomic groups Annellida, Mollusca and Crustacea. These groups belong to phyla, families and even genera with wide distributions in other latitudes; they also share dispersion characteristics and survival strategies. According with Nonato et al. (2000), the species found in the area of this study are the same ones observed in similar substrata elsewhere, indicating homogeneity of the Antarctic Peninsula's benthic fauna. This is also in accordance with the results of the present work where the occurrence of the taxonomic groups revealed high taxonomic similarity of benthic composition in both sediment types within the sites studied. Lee et al. (2001) observed 92.5% removal of metazoans density by iceberg scouring. Peck et al. (1999) reported removal of 99.5% of the whole macrofauna of soft substratum by icebergs in a depth of 9 m, while the faunal composition of the adjacent area was not affected. The observation that Polychaete, Amphipoda and Isopoda families, as well as bivalves in the adjacent area were not affected by the iceberg is consistent with the results of this study. Disturbances from ice impact could affect the colonization process however during the 18 months of the present experiment icebergs or bergy bits (blocks of ice) in the area of the experiment were not observed. But results of areas with no ice impact may be compared with our results of natural sediment. Even though during the 18 months of the present experiment icebergs or bergy bits (blocks of ice) were not observed, our results are important in the evaluation of faunal recovery in the event of ice scour in the region. According to Nonato et al. (2000) ice scour is common at 18 m in this region. The benthic community structure is determined by the recruits' supply, including mechanisms of larvae transport, settlement success and post-larval processes (Olafsson et al., 1994). However, in the present study, we could only quantify the surviving individuals at the sampling intervals; likely the great majority juveniles or adults, and the elements of mortality post-settlement, could not be evaluated in this study. Higher richness was observed in the overall periods of the natural sediment while abundance diminishes from T0 to T18 due, most probably to ecological interaction. Also richness in the defaunated sediment of T18 was similar to the natural sediment. Shannon diversity index was higher in defaunated sediment in the period T18 indicating an association with ecological interaction and if the experiment lasted for a longer period this index would, most probably, reach the natural sediment values. Polychaetes diversity increased up to 18 months surpassing natural sediment density indicating a tendency to equilibrium. The massive occurrence of Oligochaete Torodrilus sp. in most of the natural sediment periods and it's no significant occurrence in the defaunated sediment may be related to their inability to surpass a physical barrier like the boxes border that was 1 cm above the sediment. This could also have happened with some accidental species registered in the natural sediment but as their statistical relevance was not significant would be hard to analyze the effect on other species. The results obtained in this work indicate a slow colonization in the soft-sediment, consistent with that observed in hard substrata experiments (natural or artificial) (Barnes, 1996; Stanwell-Smith and Barnes, 1997). Colonization by larval dispersion is a slow process in Antarctic waters even though larvae are present almost all year around (Freire et al., 2006). Locomotion or advection probably were the most common colonization processes displayed by the fauna in defaunated sediment
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
9
Fig. 8. NMDS ordination of some relevant taxa. Dark gray circles represent a quantitative measure of each variable.
since species with higher mean relative abundance were common in both natural and defaunated sediment at initial, 6, 12 and 18 months.
Peck et al. (1999) results showed no significant recovery by Yoldia eightsi after 250 days of observation contrary to our results where Yoldia eightsi colonized defaunated sediment after 6 months.
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Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
Table 7 Relative contribution of macrofaunal species to soft sediment type according to SIMPER analysis. Sediment
Specie
Mean abundance
%Contribution
%Cumulative
natural
Torodrilus sp. Leuconidae morphotype 1 Yoldia eightsi Mysella miniuscula Cheirimedon femoratus Gamaropsis georgianus Thyasira falklandica Onoba turqueti Cirriformia sp. Priapulus tuberculatospinotus Uristes georgianus Dorvilleidae morphotype 1 Rhodine sp. Laevilitorina antarctica Apistobranchus glacierae Pseudocythereis spinifera Ophionotus victoriae Leuconidae morphotype 1 Yoldia eightsi Cheirimedon femoratus Mysella miniuscula Onoba turqueti Torodrilus sp. Thyasira falklandica Amauropsis rossiana Gamaropsis georgianus Ophelina sp. Doloria isaaczi Apistobranchus glacierae Heterophoxus videns Uristes georgianus Cirriformia sp.
9.23 4.76 4.38 3.12 2.65 1.88 1.71 1.43 1.22 0.87 0.93 0.79 0.77 0.89 0.58 0.6 0.84 6.36 5.75 6.56 3.9 2.24 1.83 1.48 2.48 1.81 1.32 1.44 0.88 1.06 0.88 0.73
25.59 12.78 12.04 6.86 5.13 4.95 3.69 3.11 2.95 2.38 2.2 1.75 1.74 1.65 1.5 1.48 1.33 18.56 18.49 9.6 8.56 6.2 5.38 4.73 3.4 2.99 2.44 2.22 2.2 2.05 1.99 1.65
25.59 38.37 50.41 57.27 62.41 67.36 71.05 74.15 77.1 79.49 81.68 83.43 85.17 86.82 88.32 89.8 91.13 18.56 37.05 46.65 55.21 61.41 66.79 71.52 74.92 77.9 80.34 82.56 84.76 86.82 88.81 90.46
defaunated
The two more common species of crustaceans (Leuconidae morphotype 1 and Cheirimedon femoratus), are both vagile, opportunists, with population distributions characterized by high concentration of individuals in small areas, scattered inside of a bigger area. This appears to be a successful survival strategy in environments with frequent disturbances caused by ice, due to high mobility characteristic and response to mechanical stimulus, as well as its reproductive pattern, where the liberation of the offspring takes place when the individuals are already formed. This same pattern of care of offspring can be seen in the bivalve Mysella miniuscula that had no difficulty in colonizing the defaunated sediment with a relative contribution of 8.6%, well above the 6.9% in the natural sediment. According to Peck et al. (1999) three major mechanisms can be identified for recolonization on shallow soft sediments: locomotion, dispersal by water currents and via larval recolonization. In the present study all three factors may have influenced recolonization of the defaunated sediment. The results of Freire et al. (2006), indicate a marked seasonality of reproductive events in Admiralty Bay, with larvae found in the water column at the end of the winter and beginning of Antarctic summer, and a consequent succession in the occurrence of pelagic larvae of benthic invertebrates in the shallow coastal zone of Martel Inlet during summer. The dynamics of the atmospheric circulation of the Antarctic Peninsula, extremely unstable and with strong displacements of air masses, that favors storm formation with winds of up to 148 km/h, has a strong influence in the destabilization of the upward layers of sediment, contributing to an increase of organism advection and subsequent restructuring of the macrofauna associations (Peck et al., 1999). 5. Conclusion The recovery observed in the abundance of the benthic community of the studied area, in relation to the levels found in the initial natural soft sediment was observed for the periods of 6, 12 and 18 months, species richness and abundance in defaunated treatment was less
than in natural treatment. The most abundant taxonomic groups were Annellida, Mollusca and Crustacea, with a wide distribution in other latitudes, were also common in Admiraty Bay. Torodrilus sp., was the most abundant species during the experiment in the natural sediment. The existence of an artificial barrier of 1 cm of height in defaunated sediment boxes may have prevented movement of the oligochaete Torodrilus sp. into the boxes, thereby accounting for the significant differences observed. If that barrier were not present these organisms would be capable to colonize the defaunated sediment in about six months, thus eliminating the differences in the composition of the associations and relative contribution of the species between the natural and defaunated sediment. Higher richness was observed in all periods of the natural sediment while abundance diminishes from T0 to T18 due, most probably to ecological interaction, also richness in the defaunated sediment of T18 was similar to the natural sediment.
Acknowledgments The field and laboratory work was financially supported by CNPq (Conselho Nacional de Pesquisa — Proc. 680044/00-0) and PROANTAR (Brazilian Antarctic Program) and the Brazilian Navy. Special thanks are due to the crew of the Skua boat for help with the fieldwork. The authors are grateful to the SCUBA divers Prof. Dr. Paulo Cesar de Paiva, Cap. Luiz Cezar Freire and Maurício Gil Vianna. We also thank Prof Dr Edmundo Ferraz Nonato and Dr Verônica Maria de Oliveira for the polychaete identification, Prof Dr Maria Teresa Valério Bernardo and Carina Waitman Rodrigues for the crustaceans identification and especially to Professor Pamela Hallock Muller from the College of Marine Science, University of South Florida, for the English review. The research reported in this paper was a part of the principal author's Master degree work in the Post-Graduation Course in Coastal and Oceanic's System (PGSISCO).[SS]
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
Appendix A. Taxonomic groups
Phylum ANNELIDA Class Oligochaeta Torodrilus sp. Class Polychaeta Dorvilleidae morphotype 1 Family Cirratulidae Cirriformia sp. Family Flabelligeridae Diplocirrus sp. Family Orbiniidae Haploscoloplos sp. Leitoscoloplos sp. Family Opheliidae Ophelina sp. Family Apistobranchidae Apistobranchus glacierae Hartman, 1978 Family Maldanidae Rhodine sp. Maldanidae morphotype 2 Family Paraonidae Levinsenia gracilis (Tauber, 1879) Family Capitellidae Capitella perarmata (Gravier, 1911) Family Syllidae Erinaceusyllis cryptica Ben-Eliahu, 1977 Family Spirorbidae Spirorbis nodenskjoldi Ehlers, 1900 Phylum MOLLUSCA Class Bivalvia Family Yoldiidae Yoldia eightsi (Couthouy,1839) Family Thyasiridae Thyasira falklandica (E.A.Smith,1885) Family Philobryidae Philobrya sublaevis (Pelseneer,1903) Family Montacutidae Mysella miniuscula (Pfeffer, 1886) Family Thraciidae Thracia meridionalis E.A.Smith,1885 Family Laternulidae Laternula elliptica (King & Broderip 1831) Class Gastropoda Family Rissoidae Onoba turqueti Lamy,1905 Family Littorinidae Laevilitorina antarctica (Smith, 1902) Family Nacellidae Nacella concinna (Strebel, 1908) Family Ampullinidae Amauropsis rossiana Smith, 1907 Family Trochidae Margarites refulgens (Smith,1907) Phylum ARTHOPODA Subphylum Crustacea Class Malacostraca Order Cumacea Leuconidae morphotype 1 Order Amphipoda Family Lysianassidae Cheirimedon femoratus (Pfeffer 1888) Family Corophiidae Gammaropsis georgianus Schellengerg, 1926 Family Uristidae Uristes georgianus Schellengerg, 1931 Family Phoxocephalidae Heterophoxus videns Barnard, 1930 Family Calliopiidae Oradarea Walker, 1903 Oedocerotidae morphotype 1 Order Isopoda Family Serolidae Serolis polita (Pfeffer, 1887) Serolidae morphotype 2 Family Munnopsidae Echinozone aries (Vanhoffen, 1914)
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Appendix A (continued) Phylum ARTHOPODA Subphylum Crustacea Class Malacostraca Order Ostracoda Family Hemicytheridae Pseudocythereis spinifera Skogsberg, 1928 Family Cypridinidae Doloria isaaczi Kornicker, 1971 Phylum ECHINODERMATA Class Echinoidea Family Cidaridae Ctenocidaris speciosa Mortensen,1910 Class Ophiuroidea Family Ophiuridae Ophionotus victoriae Bell, 1902 Phylum NEMERTEA Family Lineidae Parborlasia corrugatus (McIntosh,1876) Family Amphiporidae Amphiporus lecointei (Bürger,1904) Phylum PRIAPULIDA Family Priapulidae Priapulus tuberculatospinotus Baird,1868
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Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe
Colonization of soft sediments by benthic communities: An experimental approach in Admiralty Bay, King George Island Yargos Kern a,⁎, André Rosch Rodrigues b, Theresinha Monteiro Absher a a b
Universidade Federal do Paraná, Centro de Estudo do Mar, Laboratório de Moluscos Marinhos, Av. Beira Mar s/n, 83255–976 Pontal do Paraná, PR, Brazil Universidade de São Paulo, Instituto Oceanográfico, Departamento de Oceanografia Biológica, 05508–900 São Paulo, SP, Brazil
a r t i c l e
i n f o
Article history: Received 30 September 2013 Received in revised form 20 December 2013 Accepted 23 December 2013 Available online 19 January 2014 Keywords: Antarctica Colonization Macrobenthos Soft-sediment
a b s t r a c t In order to understand nearshore biological community colonization following impact events that affect the distribution and occurrence of species and subsequent recovery a manipulative experiment was set up in King George Island. This work aimed to study colonization patterns of benthic macrofauna in defaunated soft sediment, comparing them with occurrence patterns of macrofaunal benthic organisms found in the natural soft sediment of adjacent areas, in shallow waters of Admiralty Bay, King George Island, Antarctic Peninsula. For this, a manipulative field experiment was installed through SCUBA diving at 22 m depth in front of the Antarctic Brazilian Station. Samples of defaunated and natural soft-sediments were analyzed. Defaunated soft sediment in plastic boxes (a = 0.02 m2) were deployed in the seabed and examined after 6, 12 or 18 months. Natural soft-sediment collected with cylindrical corers of 10 cm in diameter (a = 0.08 m2), in adjacent areas at the experiment installation and during the changing and removal of the experimental boxes, were also analyzed. Altogether, 20,680 organisms belonging to 6 phyla among 42 species were identified. Thirty three taxa out of the 42 recorded were common in both natural and defaunated sediment types, 6 taxa occurred only in natural sediment and 3 taxa only in defaunated sediment. The most abundant groups throughout the experiment were: Oligochaeta, Polychaeta, Bivalvia, Gastropoda and Crustacea. In the natural sediment a total of 10 species were considered Constant, 8 species Accessory, 21 species Accidental. In the defaunated sediment 14 species were Constant, 4 species Accessory, 18 species Accidental. Analysis of variance indicated significant differences in total abundance and in Torodrilus sp. abundance in the periods of 6 and 18 months, and MDS analysis showed a clear separation between natural and defaunated treatments. Torodilus sp. was the taxon with the highest relative contribution (26%) in natural sediment. In the defaunated sediment treatments, the most common taxa were cumacean Leuconidae morphotype 1 (19%) and the bivalve Yoldia eightsi (Couthouy, 1839) (18%). The statistical results indicated significant differences between the natural and defaunated treatments with respect to benthic macrofaunal associations. Species richness and abundance in defaunated treatment were less than in natural treatment. The results suggest that recovery levels in Antarctic waters after events of defaunation are very low and in order to be of value experiments may need to be for longer periods. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Recruitment to the substratum is a crucial event in the life cycle of benthic marine invertebrates when organisms are changing in habitat and life style by settlement and early development (Stanwell-Smith and Barnes, 1997). Studies of benthic species generally consider that new settlers can arrive at a place by two main ways: 1) recruitment of pelagic larvae; 2) migration of juvenile and adults from nearby areas (Smith and Brumsickle, 1989). The life cycle of benthic species can include the indirect development with planktonic larvae (planktotrophic or lecithotrophic), the direct development with incubation of embryos and hatching of ⁎ Corresponding author. Tel.: +55 4291024673. E-mail address: [email protected] (Y. Kern). 0022-0981/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jembe.2013.12.019
juveniles' forms, or mixed development, of various incubation degrees and hatching stage of larvae (Absher et al., 2003; Barnes et al., 1993; Giese and Pearse, 1977; Hoffman et al., 2013; Peck, et al., 2006). Larval-stage duration depends on many related factors, for instance, egg type and food availability and physical-chemical conditions of seawater. Metamorphosis may happen before, during or after settlement, and in all cases the larvae becomes negatively phototactic and/or positively geotactic and goes to the sea bottom. The larva tests the physical, chemical and biological conditions of the substratum and when finding a suitable situation, completes its metamorphosis (Brusca and Brusca, 1990). Larvae are present in the water column all year round in Antarctica (Bowden et al., 2009) and settlement of some groups occurs over different periods (Pearse et al., 1991, Bowden et al., 2006). In Admiralty bay, with the beginning of the austral summer (November to March),
2
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
Fig. 1. EACF location in Martel Inlet (modified from Simões et al., 2004).
begins the supply of larvae or juveniles from the water column or sediment from adjacent areas (Freire et al., 2006). The success of larval recruitment may be affected by several factors, including the presence of adults, the hydrodynamic properties of the area, the existence of chemical traces, or some combination of these factors. While larval supply may
Table 1 Dates of installation, retrieval, time of permanency and boxes numbers of the colonization experiment in defaunated sediment. Installation
Retrieval
Permanency
Area
Box no.
December 2002 December 2003 December 2002
December 2003 June 2004 June 2004
12 months 6 months 18 months
I–III Ib–IIIb II–IV
1 to 4–9 to 12 1b/4b–9b/12b 5 to 8–13 to 16
be limiting or not, the success in the species colonization depends on the nature of the existing community together with the attributes of the local substratum, as, for instance, its stability (Constable, 1999). Processes that govern the survival and dispersion of planktonic larvae in the water column are very different from the mechanisms of substratum selection, metamorphosis and settlement of larvae, with transitional behavior occurring between planktonic and benthic stages. Substratum colonization during this period is complex, with dominance patterns and composition of the benthic community changing through time (Bromberg et al., 2000; Nonato et al., 1992). The importance of studies coupling the distribution of established taxa and substratum colonization in ecology of benthic invertebrates has been recognized since the adults' populations are linked by the dispersion of the larval stages (Bostford et al., 1994).
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
3
Table 2 Dates of natural sediment removal, period, experimental area and corer numbers.
Fig. 2. Chronological sequence of the periods of placement and retrieval of the plastic boxes for the colonization experiments of defaunated soft sediment.
The absence of a biologically relevant bathymetric variation in temperature allows a majority of Antarctic benthic species to occupy a very wide distributional pattern. Several species, whose occurrence is characteristic of shallow waters elsewhere, can extend to 500 to 1000 m of depth (Arntz et al., 1994). Moreover, in the shallow coastal zone distributions are more complex, not only exhibiting vertical zonation (Bromberg et al., 2000), but also a complex patchy distribution pattern (Bromberg et al., 2000; Nonato et al., 2000). Shallow-water colonization patterns in Admiralty Bay are especially influenced by the mechanical effect of ice. This can include the freezing of the intertidal area, as well as the impact of icebergs, evidenced by scars, disturbing or even removing benthic organisms, creating a community mosaic with different stages of succession (Dayton et al., 1974). Natural communities form those mosaics and they tend to vary unpredictably in time and space. That variability can be measured by changes or differences in the abundance of species, or in the diversity of the association (Underwood et al., 2000). Iceberg scour has been described as a major source of disruption of Antarctic near shore marine communities (Barnes and Clarke, 1994; Peck and Bullough, 1993; Rauschert, 1991). Benthic, shallow-water communities are composed by organisms of long life (Arntz et al., 1994; Clarke, 1996) and their recovery from ice impacts may take years (Arntz et al., 1994). To understand the significance of disturbance events and of benthic macrofaunal patterns of colonization requires carefully constructed colonization experiments, but such experiments are practically nonexistent in the Antarctic coastal
Date
Period
Area
Corers no.
December 2002 December 2003 December 2003 June 2004 June 2004 June 2004 June 2004
Initial (T0) 12 months (T12) 12 months (T12) 6 months (T6) 6 months (T6) 18 months (T18) 18 months (T18)
I, II, III, IV I III I III II IV
8 in each area 8 8 8 8 8 8
ecosystems (Arntz et al., 1994). The few previous studies reported (Barnes, 1996; Dayton, 1989; Rauschert, 1991) have suggested that recruitment levels in Antarctic waters are very low and that to be of value, settlement experiments may need to be immersed for extended periods. Assessing colonization patterns of the benthic macrofauna in Admiralty Bay is one of the first steps to determine the factors that contribute to or disturb the resilience and persistence of those communities. The differences observed in the communities of Antarctic shallow waters over time depend on when the disturbance occurred, relative to the availability of larvae and juveniles for colonization (Nonato et al., 2000). If the availability of larvae and juveniles varies during the austral summer, communities in which the composition and dominance are different may result, creating a faunistic mosaic in the shallow coastal zone. Slow growth, maturation and great longevity are characteristics of the Antarctic benthic macrofauna that are influential in the colonization dynamic (Arntz et al., 1994). Colonization by benthic macrofauna in experimental panels or in hard substrata has been performed in recent years in Antarctica (Barnes and Conlan, 2007 for review). However, manipulative experiments for the study of soft sediment colonization by macrobenthic fauna are a rare practice in Antarctic shallow waters. In the Arctic environment Veit-Köhler et al. (2008) studied meiobenthic colonization in soft-sediments in Kongsfjorden (Svalbard). Data obtained by this type of research permits the evaluation of the communities' recovery capacity as well as the efficiency of the species dispersion processes. This study is a first step to determine factors that contribute to or disturb the resilience and persistence of soft-sediment benthic communities in Antarctic shallow coastal waters. A manipulative field experiment was used to assess whether benthic invertebrate fauna colonized defaunated sediment at the same temporal pattern as natural sediment. The experiment allowed the evaluation of colonization pattern and community structure after 6, 12 and 18 months of a field experiment as an indication of recovery in the event of iceberg scouring in the area. The goals of our study were to determine temporal patterns of colonization of marine benthic fauna in experimentally defaunated soft sediments and to compare those with patterns of occurrence of benthic fauna in natural soft sediments from adjacent areas. The aim was to test the hypothesis that there will be differences in the composition of the benthos between the natural and defaunated soft sediment. 2. Material and methods 2.1. Study area
Fig. 3. Schematic placement of the boxes with defaunated sediment and areas of natural sediment sampling with corers.
Martel Inlet (Fig. 1), where the Brazilian Antarctic Station “Comandante Ferraz” (EACF) (62°05′S–58°23′W) is located, has a maximum depth of about 250 m. The bottom topography in front of the station includes a steep slope down to 30 m, with multiple deep scours and troughs from ice action at a depth around 18 m. In general, the sediments include gravely sand at 6 m, becoming muddy sand at 30 m (Nonato et al., 2000). At about 22 to 25 m, a plateau is formed by medium silt (Bromberg et al., 2000). This area, apparently less subject to the impact of blocks of ice, presents a muddy bottom with an abundant sessile fauna (Nonato et al., 2000). This nearshore zone
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Table 3 Constancy index of taxonomic groups in natural and defaunated sediment. Taxonomic groups
Constancy index in natural sediment
Constancy index in defaunated sediment
Torodrilus sp. Dorvilleidae morphotype 1 Cirriformia sp. Diplocirrus sp. Haploscoloplos sp. Leitoscoloplos sp. Ophelina sp. Apistobranchus glacierae Hartman, 1978 Rhodine sp. Maldanidae morphotype 2 Levinsenia gracilis (Tauber, 1879) Capitella perarmata (Gravier, 1911) Erinaceusyllis cryptica Ben-Eliahu, 1977 Spirorbis nodenskjoldi Ehlers, 1900 Yoldia eightsi (Couthouy,1839) Thyasira falklandica (E.A.Smith,1885) Philobrya sublaevis (Pelseneer,1903) Mysella miniuscula (Pfeffer, 1886) Thracia meridionalis E.A.Smith,1885 Laternula elliptica (King & Broderip 1831) Onoba turqueti Lamy,1905 Laevilitorina antarctica (Smith, 1902) Nacella concinna (Strebel, 1908) Amauropsis rossiana Smith, 1907 Margarites refulgens (Smith,1907) Leuconidae morphotype 1 Cheirimedon femoratus (Pfeffer 1888) Gammaropsis georgianus Schellengerg, 1926 Uristes georgianus Schellengerg, 1931 Heterophoxus videns Barnard, 1930 Oradarea Walker, 1903 Oedocerotidae morphotype 1 Serolis polita (Pfeffer, 1887) Serolidae morphotype 2 Echinozone aries (Vanhoffen, 1914) Pseudocythereis spinifera Skogsberg, 1928 Doloria isaaczi Kornicker, 1971 Ctenocidaris speciosa Mortensen,1910 Ophionotus victoriae Bell, 1902 Parborlasia corrugatus (McIntosh,1876) Amphiporus lecointei (Bürger,1904) Priapulus tuberculatospinotus Baird,1868
Constant Accessory Constant Accidental Accidental Accidental Accessory Accessory Accessory Accidental Accidental – Accidental Accidental Constant Constant Accidental Constant Accidental Accidental Constant Accessory Accidental Accidental – Constant Constant Constant Accessory Accidental Accidental Accidental Accidental – Accidental Accessory Accidental Accidental Accessory Accidental Accidental Constant
Constant Accidental Constant Accidental Accidental Accidental Constant Constant Accidental Accidental – Accidental Accidental Accidental Constant Constant – Constant Accidental Accidental Constant – Accidental Constant Accidental Constant Constant Accessory Constant Constant Accessory Accidental Accidental Accidental – Constant Accessory – Accidental Accidental – Accessory
of Martel Inlet at 22 m depth was the site selected for an experiment to assess the benthic macrofauna colonization.
2.2. Experimental protocol During the XXI OPERANTAR (summer 2002/2003) the experiment was deployed by SCUBA divers in front of the Brazilian Antarctic Station (62°05′11.5″S–58°23′32.9″W). The sediment to be used in the experiment was collected at 22 m in an adjacent area using a van Veen grab. After defaunation by microwave under maximum power for 30 minutes, this sediment was examined and all animals remains Table 4 Occurrence of taxonomic groups only in natural or defaunated sediment. Taxonomic group
Natural (6)
Levinsenia gracilis (Tauber, 1879) Capitella perarmata (Gravier, 1911) Philobrya sublaevis (Pelseneer,1903) Laevilitorina antarctica (Smith, 1902) Margarites refulgens (Smith,1907) Serolidae morphotype 2 Echinozone aries (Vanhoffen, 1914) Ctenocidaris speciosa Mortensen,1910 Amphiporus lecointei (Bürger,1904)
Accidental
Defaunated (3) Accidental
Accidental Accessory Accidental Accidental Accidental Accidental Accidental
removed (including dead shells), sieved through 200 μm mesh and them distributed into 16 plastic boxes (0.17x0.12x0.10 m dimensions, with volume of 0.002 m3) and covered until placement on the sea floor (T0).The borders of the plastic boxes were set about 1 cm above the surface of the local sediment. Sediment analysis indicated the presence of silt sand sediments with poor organic matter content (5.00%) in the area of installation of the experiment. The overall area of the experiment was 9 square meters. The installation of the boxes, their removal, replacement and respective placement periods in the seabed, are indicated in Table 1. The chronological sequence of the periods and areas of settlement of the boxes are indicated in the Fig. 2. These boxes, according to their numbers and positioning, stayed buried in the sediment for periods of 6 (T6), 12 (T12) and 18 (T18) months. At the end of each period the boxes were removed by SCUBA divers, covered with a plastic lid underwater and transported to the EACF laboratory. Sediment samples were sieved through 200 μm mesh and preserved in 4% buffered formaldehyde. Organisms in the samples were sorted to the lowest possible taxonomic level (no dead shells were counted). The Fig. 3 illustrates the schematic positioning of the experiment, including the location of the plastic boxes in the sampling areas (area I, II, III and IV). Natural sediment samples taken outside the area of the boxes were collected with a cylindrical corer of 10 cm diameter buried 10 cm in the sediment. Eight replicates at each site, totaling 32 samples per
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
5
800
N 700
indivíduals / 0,1m2
D 600 500 400 300 200 100 0 I
II
III
IV
T0
I
III T6
I
III T12
II
IV T18
Fig. 4. Average and standard deviation of the number of individuals/0.1 m2, where: N = natural sediment, D = defaunated sediment; period T0 = initial, T6 = 6 months, T12 = 12 months and T18 = 18 months; and respective sampling areas.
period (T0, T6, T12, and T18) were taken. Core samples were processed using the same methods described above for the experimental treatments (Table 2). The surface area of one box (0.02 m2) corresponds, approximately, to the surface area of 2 corers (0.016 m2), and consequently, the surface area of the 4 boxes of an area (0.08 m2) corresponds to the surface areas of 8 corers (0.064 m2). 2.3. Data analyses The specimens were counted and identified to the lowest possible taxonomic level based on morphological characters and specialized literature (Absher and Feijó, 1998; Sieg and Wägele, 1990). Polychaetes were identified by Prof Dr Edmundo Ferraz Nonato of Instituto Oceanográfico (Universidade de São Paulo) and Dr Verônica Maria de Oliveira (Curso de Pós-Graduação em Zoologia, Universidade Federal do Paraná), crustaceans by Prof Dr Maria Teresa Valério Bernardo and Carina Waitman Rodrigues from Centro de Estudos do Mar (Universidade Federal do Paraná). Those data were then used to calculate the number of taxa, species richness (S), relative abundances (N) and Shannon diversity index (H′). For density, a matrix with the mean number of individuals from the replicates of all samples and respective treatments was organized. The quantitative results were then transformed in densities of individuals per 0.1 m2, according with the following: 2
D ¼ n x 0:1m =A where D = density, n = mean number of individuals per sample and A = total surface area of corers (0.064 m2) or boxes (0.08 m2) of a sampling area. The classification of Bödenheimer (1955) was used to determine the Constancy Index of species, relating the number of individuals of a species to the total number of samples. The following expression was used: Ci ¼ Si =nð100Þ where Ci = Constancy Index for species i, Si = number of samples with species i, n = total number of samples. This Index identifies the species as Constant when the percentage of occurrence is ≥50%; as an Accessory species when the occurrence percentage lies between 25 and 50%; and Accidental species, when the percentage of occurrence is ≤25%. For parametric statistical analyses, matrices of abundances of the species for each period (T6, T12 and T18), for treatment/period/area were built based on the standardization of the data in individuals/ 0.1 m2. The significance level adopted was α = 0.05 for all the tests.
The possible differences among biological variables in the natural and defaunated treatments were compared through ANOVA blocks design (Underwood, 1997), adopting the treatments (natural initial, final and defaunated) and periods (T6, T12 and T18) of sampling as fixed factors. The test a posteriori LSD (Least Significant Difference) was chosen for the comparison of the averages and was applied to all values of p. Prior to ANOVA, Levene's test was employed to test the homogeneity of variances and log (x + 1) transformation of the data was applied in cases of heterogeneity. Matrices were constructed using the Bray–Curtis similarity measure on log (x + 1) to normalize organisms' counts. Species-abundance data were calculated for samples and subjected to Q-mode cluster analysis to define assemblages. The Bray–Curtis distance was used to measure proximity between samples, and Ward's linkage method was used to arrange samples into a hierarchical dendrogram. The biological data were coordinated by non-metric multidimensional scaling (NMDS) (Dufrêne and Legendre, 1997) to emphasize the geometrical aspects of similarity and to enable visualization of complex data in a graphical environment. This approach highlights patterns that might not be apparent in cluster analysis and results in a map in which the placement of samples reflects the similarity of their biological communities and environmental patterns rather than their geographical location. The NMDS efficiency is demonstrated by the stress, that represents the necessary adjustment to represent the community in few dimensions (stress ≤ 0.2 = good ordination). The analysis of Similarity Percentage (SIMPER) was used to arrange into a hierarchy the species that contributed most to the similarity among the groups. 3. Results 3.1. Fauna A total of 20,680 individuals belonging to 42 taxonomic groups and 6 phyla were identified (Appendix A). Species of Oligochaeta, Polychaeta, Bivalvia, Gastropoda and Crustacea were the most abundant (Table 3). Thirty three taxa out of the 42 recorded were common in both natural and defaunated sediment types, 6 taxa occurred only in natural sediment and 3 taxa only in defaunated sediment (Table 4). In the natural sediment a total of 10 species were considered Constant, 8 species Accessory, 21 species Accidental. In the defaunated sediment 14 species were Constant, 4 species Accessory, 18 species Accidental. Torodrilus sp. of the Phylum Annelida, class Oligochaeta was the most frequent in all the treatments, and was a Constant species on both natural and defaunated sediments. Of thirteen identified
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Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
Fig. 5. Abundance of the groups in natural sediment in the initial period (T0).
Polychaeta species in 11 families, only Cirriformia sp. was Constant in the two sediment types, 2 species (Ophelina sp. and Apistobranchus glacierae Hartman, 1978) were Constant in natural sediment, and the remaining ones were considered Accessory or Accidentals. In Phylum Mollusca, both bivalves and gastropods were recorded. In the Class Bivalvia, 4267 individuals occurred from 4 families and 7 species. Yoldia eightsi was the more abundant (2409 individuals) species, followed by Mysella miniuscula (Pfeffer, 1886) (1454 individuals) and Tyasira falklandica (Smith, 1885) (358 individuals). Those three species were considered Constant in both sediment types. In the Class Gastropoda, 5 families were represented by a total of 804 individuals. Onoba turqueti Lamy,1905 was the only Constant species in the 2 sediment types, Amauropsis rossiana Smith, 1907 was Constant in natural sediment and the remaining species were considered Accessory, Accidental or absent. Among the crustaceans, the Amphipoda were most abundant, with 3684 individuals in 6 families with one species each. Cheirimedon femoratus (Pfeffer 1888) and Leuconidae (morphotype 1) were the only Constant species in the two sediment types, Gammaropsis georgianus Schellengerg, 1926 was Constant in natural sediment and Uristes georgianus Schellengerg, 1931 was Constant in defaunated sediment. In the order Isopoda, only 46 individuals in 3 families were represented by Accessory or Accidental species. The Class Ostracoda was represented by 311 individuals. The family Hemicyteridae (266 individuals) and
only one species, Pseudocythereis spinifera Skogsberg, 1928, was Constant in defaunated sediment. The family Cypridinidae (45 individuals) was represented by the species Doloria isaaczi Kornicker, 1971. The other groups, such as the Echinodermata, Nemertinea and Priapulida, were relatively rare. The specie Ctenocidaris speciosa Mortensen, 1910 (Echinodermata) occurred only once and the ophiuroid Ophionotus victoriae Bell, 1902 had a frequency of 115 individuals and was an Accessory specie in natural sediment and Accidental in defaunated sediment. The individuals from the Phylum Nemertea represented the families Lineidae, with the species Parborlasia corrugatus (McIntosh,1876) with 24 individuals, and Amphiporidae, with the species Amphiporus lecointei (Burger, 1904) with 4 individuals. The Phylum Priapulida had a total frequency of 75 individuals, all of the same species, Priapulus tuberculatospinotus, Baird, 1868, which considered Constant in natural sediment and Accessory in defaunated sediment. 3.2. Density and abundance Species with higher mean relative frequencies in natural sediment were: Oligochaeta Torodrilus sp (47.7%), Cumacea Leconidae morphotypy 1 (12.8%), Bivalvia Yoldia eightsi (12.0%). In defaunated sediment species with higher relative abundance were after 6 months: Amphipoda Cheirimedon femoratus (24.4%), Cumacea Leuconidae morphotype 1 (20.2%), Bivalvia Mysella miniuscula (14.4%) and Yoldia eightsi (12.6%)
Fig. 6. Abundance of Annelida, Mollusca and Crustacea in natural and defaunated sediment per periods and areas; N — natural, D — defaunated; period T6 — 6 months; T12 — 12 months; T18 — 18 months.
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
7
Table 5 Summary of ANOVA and test a posteriori (LSD), considering as factor the period and treatment (i = natural initial, f = natural final, d = defaunated) and as variables the community's structural parameters (abundance, richness, diversity). T6 = period of 6 months, T12 = period of 12 months and T18 = period of 18 months. T6
Abundance Error LSD test Richness Error LSD test Diversity Error LSD test
T12
T18
MS
F
p
MS
F
p
MS
F
p
320,862 98,140
3.269
0.0496
176,392 191,593
0.921
0.4074
136,660 49,053
2.786
0.0767
(f N d) = i 1.638
0.2086
fNd=i 4.167
0.0236
(f N d) = i 3.183
0.0548
fNd=i 0.886
0.4209
2.225
0.1227
(f N d) = i 1.462
0.2469
27.169 16.589 0.17670 0.19934
53.344 12.800 0.48018 0.21582
fNd=i
51.821 16.278 0.22287 0.15249
(f N d) = i
and Gastropoda Amauropsis rossiana (10.1%); after 12 months: Amphipoda Cheirimedon femoratus (47.1%), Cumacea Leuconidae morphotype 1 (21.6%) and Bivalvia Yoldia eightsi (13.4%); after 18 months: Cumacea Leuconidae morphotype 1 (34.2%), Bivalvia Yoldia eightsi (23.4%) and Amphipoda Oedoceratidae morphotype 1 (19.4%) The highest mean densities were found: a) in NT0III in the period of the experiment installation (478.7 inds/0.1 m2), b) at 6 and 12 months in defaunated sediment in samples DT6I and DT12I (453 and 460 inds/ 0.1 m2, respectively, and at 18 months in natural sediment, sample NT18IV (460 inds/0.1 m2) (Fig. 4). Mean densities in natural sediment at 6 and 12 months were similar, except for area III, that showed a variation between 415 inds/0.1 m2 (NT6III) and 220 inds/0.1 m2 (NT12III). In defaunated sediment, the density values also were similar in the two sampling periods. At 18 months, the mean density of the natural sediment macrofauna of area II showed a significant low value (139 inds/0.1 m2), when compared to the other periods. Period of 6 and 12 months of defaunated sediment showed a smaller mean values of density in area III (245 inds/o.1 m2) when compared to area I, and a similarity in area IV (208 inds/0.1 m2) with area II. Abundance of the groups in natural sediment in the initial period (NT0) of the experiment are shown in Fig. 5 and subsequent abundance of the more representative taxonomic groups Annelida, Mollusca and Crustacea are in Fig. 6. Annellida were more abundant in natural sediment in all periods. Mollusks tended to be similarly abundant in the two types of sediment. Crustaceans presented the maximum abundance value (1188 individuals) in defaunated sediment in period DT12. Echinodermata, Nemertea and Priapulida were uncommon in all samples with the exception of Echinodermata (Ophionotus victoriae — 63 individuals) in natural sediment in the period NT18. 3.3. Analysis of variance The results of the evaluation of the community's structural parameters – abundance, species richness and diversity of Shannon –
fNd=i
are presented in Table 5. Data for the most abundant organisms of the taxonomic groups Annelida, Mollusca and Crustacea (the species Torodrilus sp., Y. eightsi and Leuconidae morphotype 1 respectively) are reported in Table 6. Analysis of variance revealed significant differences in the total abundance between final natural sediment and defaunated after 06 and 18 months. This difference was the consequence of the difference in the abundance of Torodrilus sp. (dominant species of natural sediment) in these periods. Significant differences were also observed in species richness at 12 and 18 months, in diversity and in abundance of Torodrilus sp. at 12 months and Leuconidae morphotype 1 at 6 months.
3.4. Cluster groups and non-metric analysis The Q Mode cluster analysis based on the overall species and ecological indexes revealed two groups and five subgroups (Fig. 7A and B). Group 1 is composed mainly by the defaunated samples; two subgroups can be distinguished, G1-A with DT18II, DT6IIIb, DT12III and DT18IV; and G1-B with the samples DT12I and, NT0IV. Some samples of natural sediment of this area and period were lost (and were not accounted for in the estimates) that may explain the low values of abundance (see Fig. 5). Group 2 is composed of natural sediment samples with three distinct subgroups. Subgroup G2-A with the samples NT6III, NT6I and NT18IV, G2-B with the samples NT12I, NT12III, NT0II and NT0III, and G2-C with the samples NT18II and NT0I. The sample DT6Ib did not belong to any group. The NMDS analyses performed using the biological data within collected samples showed the same groups as revealed in the cluster analysis (Figs. 7C and 8). Group 1 showed the lowest abundance of specimens and high values of Shannon diversity, especially in the subgroup G1-B. Amphipoda were abundant in samples in subgroup G1-A. Group 2 showed the highest abundance, especially in the subgroup G2-A, which has a high abundance of Annelida specimens (mainly Torodrilus.sp). Isopoda were abundant in the subgroup G2-B and the subgroup G2-C showed a high abundance of Echinodermata.
Table 6 Summary of ANOVA and test a posteriori LSD, considering as factor the period and treatment (i = natural initial, f = natural final, d = defaunated) and as variables the most abundant taxa (Torodrilus sp., Yoldia eightsi, Leuconidae morphotype 1). T6 = period of 6 months, T12 = period of 12 months and T18 = period of 18 months. T6
Torodrilus sp. Error LSD test Yoldia eightsi Error LSD test Leuconidae Error LSD test
T12
T18
MS
F
p
MS
F
p
MS
F
p
229,656.7 45195.7 (f N d) = i 4031.99 1860.22 f=d=i 20,472.7 5339.5
5.08139
0.011381
2.269
0.1180
0.0300
0.129174
1.889
0.1660
0.404
0.6707
3.83423
0.030933
0.124
0.8841
89,354.4 22787.4 (f N d) = i 673.53 1665.28 f=d=i 4552.6 3882.9
3.921
2.16748
282,843 124,651 (d b i) = f 3840.73 2033.58 f=d=i 335.60 2715.32
1.172
0.3225
(i = d) b f
f=d=i
f=d=i
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(natural or defaunated). Torodrilus sp. was the dominant taxon in the natural sediment, with a relative contribution of 26%, and the crustacean Leuconidae morphotype 1, with a relative contribution of 19%, was the dominant in the defaunated sediment (Table 7). 4. Discussion
Fig. 7. Location of the boxes with natural and defaunated sediment in areas I, II, III, IV (A) and dendrogram classification (Q-mode) from abundance of species by areas and boxes (B) and NMDS of species occurrence by groups (C).
The relative contribution of the species, calculated by SIMPER analysis, among treatments and time, evaluated changes in the patterns of dominance of the macrofauna population for each sediment type
Results of the fauna composition showed 10 species to be constant representing 90% (18,640 individuals) from the total of 20,680 organisms belonging to the taxonomic groups Annellida, Mollusca and Crustacea. These groups belong to phyla, families and even genera with wide distributions in other latitudes; they also share dispersion characteristics and survival strategies. According with Nonato et al. (2000), the species found in the area of this study are the same ones observed in similar substrata elsewhere, indicating homogeneity of the Antarctic Peninsula's benthic fauna. This is also in accordance with the results of the present work where the occurrence of the taxonomic groups revealed high taxonomic similarity of benthic composition in both sediment types within the sites studied. Lee et al. (2001) observed 92.5% removal of metazoans density by iceberg scouring. Peck et al. (1999) reported removal of 99.5% of the whole macrofauna of soft substratum by icebergs in a depth of 9 m, while the faunal composition of the adjacent area was not affected. The observation that Polychaete, Amphipoda and Isopoda families, as well as bivalves in the adjacent area were not affected by the iceberg is consistent with the results of this study. Disturbances from ice impact could affect the colonization process however during the 18 months of the present experiment icebergs or bergy bits (blocks of ice) in the area of the experiment were not observed. But results of areas with no ice impact may be compared with our results of natural sediment. Even though during the 18 months of the present experiment icebergs or bergy bits (blocks of ice) were not observed, our results are important in the evaluation of faunal recovery in the event of ice scour in the region. According to Nonato et al. (2000) ice scour is common at 18 m in this region. The benthic community structure is determined by the recruits' supply, including mechanisms of larvae transport, settlement success and post-larval processes (Olafsson et al., 1994). However, in the present study, we could only quantify the surviving individuals at the sampling intervals; likely the great majority juveniles or adults, and the elements of mortality post-settlement, could not be evaluated in this study. Higher richness was observed in the overall periods of the natural sediment while abundance diminishes from T0 to T18 due, most probably to ecological interaction. Also richness in the defaunated sediment of T18 was similar to the natural sediment. Shannon diversity index was higher in defaunated sediment in the period T18 indicating an association with ecological interaction and if the experiment lasted for a longer period this index would, most probably, reach the natural sediment values. Polychaetes diversity increased up to 18 months surpassing natural sediment density indicating a tendency to equilibrium. The massive occurrence of Oligochaete Torodrilus sp. in most of the natural sediment periods and it's no significant occurrence in the defaunated sediment may be related to their inability to surpass a physical barrier like the boxes border that was 1 cm above the sediment. This could also have happened with some accidental species registered in the natural sediment but as their statistical relevance was not significant would be hard to analyze the effect on other species. The results obtained in this work indicate a slow colonization in the soft-sediment, consistent with that observed in hard substrata experiments (natural or artificial) (Barnes, 1996; Stanwell-Smith and Barnes, 1997). Colonization by larval dispersion is a slow process in Antarctic waters even though larvae are present almost all year around (Freire et al., 2006). Locomotion or advection probably were the most common colonization processes displayed by the fauna in defaunated sediment
Y. Kern et al. / Journal of Experimental Marine Biology and Ecology 453 (2014) 1–12
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Fig. 8. NMDS ordination of some relevant taxa. Dark gray circles represent a quantitative measure of each variable.
since species with higher mean relative abundance were common in both natural and defaunated sediment at initial, 6, 12 and 18 months.
Peck et al. (1999) results showed no significant recovery by Yoldia eightsi after 250 days of observation contrary to our results where Yoldia eightsi colonized defaunated sediment after 6 months.
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Table 7 Relative contribution of macrofaunal species to soft sediment type according to SIMPER analysis. Sediment
Specie
Mean abundance
%Contribution
%Cumulative
natural
Torodrilus sp. Leuconidae morphotype 1 Yoldia eightsi Mysella miniuscula Cheirimedon femoratus Gamaropsis georgianus Thyasira falklandica Onoba turqueti Cirriformia sp. Priapulus tuberculatospinotus Uristes georgianus Dorvilleidae morphotype 1 Rhodine sp. Laevilitorina antarctica Apistobranchus glacierae Pseudocythereis spinifera Ophionotus victoriae Leuconidae morphotype 1 Yoldia eightsi Cheirimedon femoratus Mysella miniuscula Onoba turqueti Torodrilus sp. Thyasira falklandica Amauropsis rossiana Gamaropsis georgianus Ophelina sp. Doloria isaaczi Apistobranchus glacierae Heterophoxus videns Uristes georgianus Cirriformia sp.
9.23 4.76 4.38 3.12 2.65 1.88 1.71 1.43 1.22 0.87 0.93 0.79 0.77 0.89 0.58 0.6 0.84 6.36 5.75 6.56 3.9 2.24 1.83 1.48 2.48 1.81 1.32 1.44 0.88 1.06 0.88 0.73
25.59 12.78 12.04 6.86 5.13 4.95 3.69 3.11 2.95 2.38 2.2 1.75 1.74 1.65 1.5 1.48 1.33 18.56 18.49 9.6 8.56 6.2 5.38 4.73 3.4 2.99 2.44 2.22 2.2 2.05 1.99 1.65
25.59 38.37 50.41 57.27 62.41 67.36 71.05 74.15 77.1 79.49 81.68 83.43 85.17 86.82 88.32 89.8 91.13 18.56 37.05 46.65 55.21 61.41 66.79 71.52 74.92 77.9 80.34 82.56 84.76 86.82 88.81 90.46
defaunated
The two more common species of crustaceans (Leuconidae morphotype 1 and Cheirimedon femoratus), are both vagile, opportunists, with population distributions characterized by high concentration of individuals in small areas, scattered inside of a bigger area. This appears to be a successful survival strategy in environments with frequent disturbances caused by ice, due to high mobility characteristic and response to mechanical stimulus, as well as its reproductive pattern, where the liberation of the offspring takes place when the individuals are already formed. This same pattern of care of offspring can be seen in the bivalve Mysella miniuscula that had no difficulty in colonizing the defaunated sediment with a relative contribution of 8.6%, well above the 6.9% in the natural sediment. According to Peck et al. (1999) three major mechanisms can be identified for recolonization on shallow soft sediments: locomotion, dispersal by water currents and via larval recolonization. In the present study all three factors may have influenced recolonization of the defaunated sediment. The results of Freire et al. (2006), indicate a marked seasonality of reproductive events in Admiralty Bay, with larvae found in the water column at the end of the winter and beginning of Antarctic summer, and a consequent succession in the occurrence of pelagic larvae of benthic invertebrates in the shallow coastal zone of Martel Inlet during summer. The dynamics of the atmospheric circulation of the Antarctic Peninsula, extremely unstable and with strong displacements of air masses, that favors storm formation with winds of up to 148 km/h, has a strong influence in the destabilization of the upward layers of sediment, contributing to an increase of organism advection and subsequent restructuring of the macrofauna associations (Peck et al., 1999). 5. Conclusion The recovery observed in the abundance of the benthic community of the studied area, in relation to the levels found in the initial natural soft sediment was observed for the periods of 6, 12 and 18 months, species richness and abundance in defaunated treatment was less
than in natural treatment. The most abundant taxonomic groups were Annellida, Mollusca and Crustacea, with a wide distribution in other latitudes, were also common in Admiraty Bay. Torodrilus sp., was the most abundant species during the experiment in the natural sediment. The existence of an artificial barrier of 1 cm of height in defaunated sediment boxes may have prevented movement of the oligochaete Torodrilus sp. into the boxes, thereby accounting for the significant differences observed. If that barrier were not present these organisms would be capable to colonize the defaunated sediment in about six months, thus eliminating the differences in the composition of the associations and relative contribution of the species between the natural and defaunated sediment. Higher richness was observed in all periods of the natural sediment while abundance diminishes from T0 to T18 due, most probably to ecological interaction, also richness in the defaunated sediment of T18 was similar to the natural sediment.
Acknowledgments The field and laboratory work was financially supported by CNPq (Conselho Nacional de Pesquisa — Proc. 680044/00-0) and PROANTAR (Brazilian Antarctic Program) and the Brazilian Navy. Special thanks are due to the crew of the Skua boat for help with the fieldwork. The authors are grateful to the SCUBA divers Prof. Dr. Paulo Cesar de Paiva, Cap. Luiz Cezar Freire and Maurício Gil Vianna. We also thank Prof Dr Edmundo Ferraz Nonato and Dr Verônica Maria de Oliveira for the polychaete identification, Prof Dr Maria Teresa Valério Bernardo and Carina Waitman Rodrigues for the crustaceans identification and especially to Professor Pamela Hallock Muller from the College of Marine Science, University of South Florida, for the English review. The research reported in this paper was a part of the principal author's Master degree work in the Post-Graduation Course in Coastal and Oceanic's System (PGSISCO).[SS]
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Appendix A. Taxonomic groups
Phylum ANNELIDA Class Oligochaeta Torodrilus sp. Class Polychaeta Dorvilleidae morphotype 1 Family Cirratulidae Cirriformia sp. Family Flabelligeridae Diplocirrus sp. Family Orbiniidae Haploscoloplos sp. Leitoscoloplos sp. Family Opheliidae Ophelina sp. Family Apistobranchidae Apistobranchus glacierae Hartman, 1978 Family Maldanidae Rhodine sp. Maldanidae morphotype 2 Family Paraonidae Levinsenia gracilis (Tauber, 1879) Family Capitellidae Capitella perarmata (Gravier, 1911) Family Syllidae Erinaceusyllis cryptica Ben-Eliahu, 1977 Family Spirorbidae Spirorbis nodenskjoldi Ehlers, 1900 Phylum MOLLUSCA Class Bivalvia Family Yoldiidae Yoldia eightsi (Couthouy,1839) Family Thyasiridae Thyasira falklandica (E.A.Smith,1885) Family Philobryidae Philobrya sublaevis (Pelseneer,1903) Family Montacutidae Mysella miniuscula (Pfeffer, 1886) Family Thraciidae Thracia meridionalis E.A.Smith,1885 Family Laternulidae Laternula elliptica (King & Broderip 1831) Class Gastropoda Family Rissoidae Onoba turqueti Lamy,1905 Family Littorinidae Laevilitorina antarctica (Smith, 1902) Family Nacellidae Nacella concinna (Strebel, 1908) Family Ampullinidae Amauropsis rossiana Smith, 1907 Family Trochidae Margarites refulgens (Smith,1907) Phylum ARTHOPODA Subphylum Crustacea Class Malacostraca Order Cumacea Leuconidae morphotype 1 Order Amphipoda Family Lysianassidae Cheirimedon femoratus (Pfeffer 1888) Family Corophiidae Gammaropsis georgianus Schellengerg, 1926 Family Uristidae Uristes georgianus Schellengerg, 1931 Family Phoxocephalidae Heterophoxus videns Barnard, 1930 Family Calliopiidae Oradarea Walker, 1903 Oedocerotidae morphotype 1 Order Isopoda Family Serolidae Serolis polita (Pfeffer, 1887) Serolidae morphotype 2 Family Munnopsidae Echinozone aries (Vanhoffen, 1914)
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Appendix A (continued) Phylum ARTHOPODA Subphylum Crustacea Class Malacostraca Order Ostracoda Family Hemicytheridae Pseudocythereis spinifera Skogsberg, 1928 Family Cypridinidae Doloria isaaczi Kornicker, 1971 Phylum ECHINODERMATA Class Echinoidea Family Cidaridae Ctenocidaris speciosa Mortensen,1910 Class Ophiuroidea Family Ophiuridae Ophionotus victoriae Bell, 1902 Phylum NEMERTEA Family Lineidae Parborlasia corrugatus (McIntosh,1876) Family Amphiporidae Amphiporus lecointei (Bürger,1904) Phylum PRIAPULIDA Family Priapulidae Priapulus tuberculatospinotus Baird,1868
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