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Marine Biodiversity

, Volume 48, Issue 1, pp 105–115 | Cite as

Assessment of ecological quality status along the Apulian coasts (eastern Mediterranean Sea) based on meiobenthic and nematode assemblages

  • Federica Semprucci
  • Maria Balsamo
  • Luca Appolloni
  • Roberto Sandulli
Meio Extreme

Abstract

Coastal environments may be impacted by several anthropogenic activities such as sewage discharges, fish-farming and hydrocarbons along with seaside tourism activities, all proved to have an effect on benthic and, particularly, meiobenthic assemblages. An ecological survey was conducted along the Apulian coast (South Italy) to explore potential relationships between the degree of human disturbance and meiobenthic communities which are still unexplored. Sediment samples were collected in triplicate from 3 stations along each of 16 transects and at a different depth gradient (from ∼10 to 50 m). The levels of taxa richness and biodiversity of the meiobenthic and nematode assemblages were overall high. The Water Framework Directive and Marine Strategy Framework Directive suggest the creation of specific thresholds to define the EcoQ (Ecological Quality) status of marine coastal systems. The thresholds applied on the meiobenthos showed the worst conditions at Brindisi harbour and at the mussel farm infrastructure of Castro. An overall moderate impact was also detected at the multiple-use Marine Protect Area of Porto Cesareo, likely due to the overwhelming number of tourists leading to an increase of organic enrichment (sewage discharge) negatively affecting the benthic communities assemblages. The main representatives of the nematode assemblages were taxa known as typical of muddy sediments. When EcoQ was assessed with the nematode thresholds, the worst EcoQ was found at Brindisi Harbour, Torre Specchia, and Alimini Lakes. The ecological conditions revealed by meiobenthic and nematode assemblages were generally consistent and seem to highlight a greater alteration of the meiobenthic communities assemblages along the Adriatic than the Ionian coasts.

Keywords

Meiobenthos Nematodes Monitoring Fauna Ecological assessment Shallow subtidal habitats 

Introduction

Human activities alter marine ecosystems at different levels making it critical to understand the consequences of possible environmental changes (Zeppilli et al. 2015; Semprucci et al. 2016). The Water Framework Directive (WFD, 2000/60/EC) was an important milestone in European environmental policies, being the result of numerous years of discussions among experts, stakeholders and policy makers. WFD and the more recent Marine Strategy Framework Directive (MSFD, 2008/56/EC) defined a roadmap that aims to the achievement or maintaining of a Good Environmental Status (GEnS) of the European seas by 2020. Both these regulations recognize that biomonitoring by means of invertebrate organisms may help to evaluate the extent of human impacts and may help to understand and control the loss of ecosystem functioning (Van Hoey et al. 2010; Semprucci et al. 2013a, 2014; Borja et al. 2014).

Meiobenthic organisms are generally considered good bioindicators in marine habitats (Kennedy and Jacoby 1999). The reason for using meiobenthos in the biomonitoring studies is based on the several advantages of this assemblage over macrobenthos, such as its high abundance and diversity, wide distribution, pervasiveness and tolerance, and also low mobility and high turnover rate (see Höss and Traunspurger 2003 for review). Within the meiobenthos, nematodes are the most relevant group in terms of diversity, abundance and wide distribution in the sediments in all habitats (e.g. Balsamo et al. 2012; Moens et al. 2013). The above-cited European directives have established the concept of Ecological Quality (EcoQ) status as a way to assess the biological quality of aquatic habitats. The EcoQ status is based upon the composition of several biological elements and organisms, and among them the meiobenthic and nematode communities assemblages may be used as possible tools to determine the EcoQ of the marine sediments (Balsamo et al. 2010; Höss et al. 2011; Semprucci et al. 2015a, b; Fonseca and Gallucci 2016).

The coastal zone is the interface between land and sea and has a central role in the social and economic development (Torre and Selicato 2013). In addition, Apulia accounts for ∼800 km of coastline, one of the largest coastal extensions in Italy. However, the meiobenthic and especially nematode assemblages of the area are still insufficiently explored (e.g. Sandulli et al. 2004, 2010; De Leonardis et al. 2008; Semprucci et al. 2014).

The present survey is the largest study on the biodiversity and ecology of meiobenthos carried out along the Italian coasts: it covers the Apulian coast between Porto Cesareo (Ionian Sea) and Torre Guaceto (southern Adriatic Sea), two important Marine Protect Areas (MPA). However, this area is subject to numerous types of anthropogenic stress such as the presence of commercial and industrial harbours, aquaculture infrastructures, urban wastewaters, agriculture drainage watercourses and areas characterized by tourist disturbance. In particular, the proliferation of tourist infrastructures in the coastal systems led to an enhancement of the pressure on sewage disposal facilities especially in localities that have a higher number of inhabitants only in the high seasons. Here, wastewater treatment facilities are often not built to cope with the rise in wastewater volumes during the peaks of tourists stay, which produce a significant impact on the flora and fauna of the marine areas surrounding the points of tourist interest (Frontalini et al. 2011). Sewage run-offs cause serious damage in particular to benthic organisms because it stimulates microalgal blooms and consequent hypoxia in the sediments (Semprucci et al. 2010a). However, the level of human pressure and the real ecological state of several localities of the Apulian coasts are not yet fully known. Furthermore, the high conservation value of this coastline, the increasing expansion of tourism activities and their possible impact make it necessary to perform an evaluation of the EcoQ in order to ensure a sustainable management of this important stretch of coast. Accordingly, the aims of the present study were to provide: (1) new information about meiobenthos and nematode fauna from a very extensive coastal area of southern Italy and (2) an assessment of the ecological state of this area, as a baseline for monitoring future changes.

Materials and methods

Study area and field activities

The study was carried out along the Apulian coast (Ionian and Adriatic seas, eastern Mediterranean Sea), where the human population has greatly increased since 1991 and touristic pressure is high especially during the summer period. This coastline includes areas of relevant conservation value, but the enhancement of human activities has led to a worsening of the environmental quality. For instance, the tourist, commercial and industrial harbour of Brindisi was included by the Italian Environmental Ministry in the list of high-risk areas mainly due to the pollution impact of the industrial centre. On the western Ionian coast, Porto Cesareo and Gallipoli have recently been subject to the construction of new large tourist infrastructures, while in the southern part of Apulia, Otranto, Lecce and Santa Cesarea are relevant tourist localities hosting in the high season up to the 70% of the tourist flow of the whole region (CoNISMa 2001).

Samples were collected in March 2000 during the INTERREG Program Italy/Greece. The sampling routine was carried out by a modified Van Veen grab along 16 transects (T) perpendicular to the coastline and at three different depths, hereafter named as stations (St. 1 ∼10 m, St. 2 ∼20 m and St. 3 ∼50 m) (Figs. 1, 2). The transects were selected to compare areas subject to a documented human impact (e.g. harbours, aquaculture infrastructures, urban wastewater and agriculture drainage watercourses) with MPAs or natural areas (e.g. Torre Guaceto, Cesine, Porto Cesareo) (see Table 1).
Fig. 1

Geographical position of the sampling stations along the Adriatic–Ionian coasts

Fig. 2

Non metric multi-dimensional scaling plots of the meiobenthic assemblages (stress level: 0.12): a compared between the various transects, b) between depths (stations), and indicated by the respective labels

Table 1

Sampling locations and main environmental features

Location

Transect

Station

Area features and assumed impact

Depth

Latitude

Longitude

Wentworth classification

(m)

Torre Guaceto

T1

1

Marine Protected Area

Low impact

13

40°43.09N

17°48.64E

Coarse sand

2

18

40°43.06N

17°49.37E

Fine sand

3

44

40°43.15N

17°51.10E

Mud

Brindisi

T3

1

Brindisi Harbour

High Impact

10

40°38.63N

17°56.69E

Mud

2

20

40°39.58N

17°59.53E

Mud

3

45

40°40.09N

17°59.77E

Mud

Mattarelle

T4

1

Electrical power station warm waters

Moderate Impact

10

40°34.35N

18°02.94E

Coarse sand

2

16

40°32.81N

18°06.29E

Fine sand

3

46

40°34.33N

18°09.60E

Mud

Lendinuso

T5

1

Area in front of an urban waste water channel

Moderate Impact

10

40°31.59N

18°05.51E

Sand

2

20

40°32.62N

18°07.08E

Fine sand

3

50

40°33.74N

18°11.17E

Mud

Cesine

T8

1

Land Nature reserve

Low Impact

10

40°22.08N

18°20.86E

Coarse sand

2

24

40°22.05N

18°21.35E

Coarse sand

3

53

40°22.55N

18°21.52E

Mud

Torre Specchia

T9

1

Area with seaside tourist impact

Moderate Impact

12

40°19.36N

18°23.16E

Fine sand

2

20

40°19.25N

18°23.42E

Fine sand

3

53

40°19.95N

18°23.80E

Mud

Baia dei laghi Alimini

T10

1

Bay with seaside tourist impact

Moderate Impact

10

40°12.16N

18°27.80E

Very fine sand

2

21

40°11.95N

18°28.26E

Sand

3

51

40°11.26N

18°30.18E

Mud

Santa Cesarea terme

T11

1

Seaside tourist impact area

Moderate Impact

20

40°01.99N

18°27.47E

n.a.

2

30

40°02.00N

18°27.65E

n.a.

3

52

40°02.05N

18°27.96E

n.a.

Castro

T12

1

Mussel farm

Moderate/high impact

15

39°59.38N

18°25.01E

n.a.

2

25

39°59.57N

18°25.51E

Fine sand

3

55

39°58.99N

18°26.52E

Mud

Gagliano

T13

1

Area with very low seaside tourist impact

Low impact

10

39°51.26N

18°23.55E

Coarse sand

2

22

39°51.54N

18°23.69E

Coarse sand

3

53

39°50.88N

18°23.65E

Mud

Santa Cesarea

T14

1

Area with low human impact

Low/moderate impact

9

39°58.71N

18°18.28E

n.a.

2

20

39°48.50N

18°18.31E

Coarse sand

3

54

39°57.33N

18°17.98E

Mud

Torre Mozza

T15

1

Small fish processing infrastructure

Low/moderate impact

14

39°50.46N

18°07.38E

Coarse sand

2

22

39°50.45N

18°06.40E

Coarse sand

3

50

39°49.99N

18°04.74E

Mud

S. Giovanni-Mancaversa

T16

1

Land Natural reserve

Low/moderate impact

11

39°55.55N

18°02.81E

Coarse sand

2

20

39°55.36N

18°02.77E

Sand

3

52

39°55.09N

18°00.76E

Coarse sand

Gallipoli

T18

1

Seaside tourist Area

Low/moderate impact

10

40°03.92N

17°59.64E

Coarse sand

2

25

40°03.62N

17°57.41E

Coarse sand

3

54

40°03.70N

17°52.97E

Mud

S. Isidoro

T19

1

Seaside tourist Area

Low/moderate impact

14

40°12.94N

17°55.07E

Coarse sand

2

21

40°13.01N

17°54.78E

Sand

3

52

40°09.45N

17°51.48E

Mud

Porto Cesareo

T20

1

Multiple-use Marine Protected Area

Low/moderate impact

15

40°15.37N

17°52.83E

Coarse sand

2

21

40°14.93N

17°53.38E

Coarse sand

3

50

40°10.52N

17°49.09E

Coarse sand

n.a. not applicable

At all stations, a sample of sediment was taken by a Van Veen grab. Down-cast and recovery speed of grab were slowed down as much as possible to minimize bow-wave resuspension effects, in accordance to Albertelli et al. (1999). Furthermore, grab was modified to permit visual examination of the sediment state through two upper ports closed by lids. Immediately after grab recovery and check of the sediment status, sediment subsamples were taken for meiofaunal analysis. In particular, subsamples were collected in 3 replicates from 3 different Van Veen grab samples by plexiglass corers (inner diameter, 2.8 cm, area 6.2 cm2) inserted down to 10 cm depth from the upper central part of grab (Albertelli et al. 1999). This procedure allows the collection of almost completely undisturbed portions of sediments (see Moreno et al. 2011 for further details).

Subsamples were treated with MgCl2 for anaesthetizing organisms and then fixed with 5% buffered formaldehyde in pre-filtered seawater solution. Additional sediment samples were collected for the grain-size analysis of sediment, using a manual corer, 2.8 cm internal diameter. Due to technical problems, no samples could be taken for grain size analysis at T11, T12 St. 1 or T14 St. 1 (see Table 1).

Grain-size analysis

For the dry-sieving analysis, sediment samples were oven dried at 80 °C for 24 h. After drying, the sediment was weighed and passed through a set of standard sediment sieves (from 0.8 mm to 0.074 mm). Sediments were classified following the Udden and Wentworth scale and the final classification is reported in Table 1 (Wentworth 1922).

Meiobenthos and nematode analyses

In the laboratory, meiobenthic organisms were sorted out by sieving the samples through a 43-μm mesh net and animal extraction was performed by flotation and multiple decantation, following the procedure described by McIntyre and Warwick (1984). As suggested by Danovaro et al. (2004), just for the muddy sediments the fraction retained by the 43-μm net was treated by Ludox AM (McIntyre and Warwick 1984). After staining with Rose Bengal (0.5 g L−1), meiobenthic organisms were counted and identified to the major taxon level, using a stereomicroscope. One hundred nematodes from each sample were randomly picked out using a fine pin under a stereomicroscope (magnification ×40), and mounted on permanent slides using anhydrous glycerine according to Seinhorst (1959), with the only exception being the specimens collected in transects T1, T4 and T8 which, due to a fixation problem, resulted in them being too damaged for a detailed taxonomical study.

Nematodes were identified to genus level using pictorial keys (Platt and Warwick 1983, 1988; Warwick et al. 1998), as well as the whole literature available on the Mediterranean area (Guilini et al. 2016). The following indices were calculated at major taxon level for meiobenthos and at genus level for nematodes: richness, Shannon–Wiener diversity index (Hˈ, log2) and Pielou-evenness (Jˈ) (Shannon and Weaver 1949; Pielou 1969). Furthermore, the Maturity Index (MI), based on the relative proportion of nematode species genera of colonizers (r-strategists) and persisters (k-strategists), was calculated in each sample (Bongers 1990; Bongers et al. 1991). EcoQ status was assessed by the number of meiobenthic taxa (richness) as suggested by Danovaro et al. (2004), modified according to WFD classes, while the threshold values indicated by Moreno et al. (2011) and Semprucci et al. (2014) were applied to assess the EcoQ with nematodes (Table 2).
Table 2

Thresholds considered to evaluate the EcoQ of the study area (see for more details Danovaro et al. 2004. Moreno et al. 2011. Semprucci et al. 2014)

Faunal parameters

High

Good

Moderate

Poor

Bad

Meiobenthic richness (S)

≥16

16< S <12

8< S <11

4< S <7

≤4

Nematode Shannon Index (H′)

>4.5

3.5< H′ <4.5

2.5< H′ <3.5

1<H′ ≤2.5

0< H′ ≤1

Nematode Maturity Index (MI)

>2.8

2.8≤ MI <2.6

2.6≤ MI <2.4

2.4≤ MI <2.2

≤2.2

Nematode c-p 1 and c-p2

0–20%

20–40%

40–60%

60–80%

80–100%

Nematode c-p 3 and c-p4

80–100%

60–80%

60–40% 40-60%

20–40%

0–20%

Statistical analysis

Differences between transects and stations were tested by a two-way ANOVA (analysis of variance) performed on meiobenthic and nematode univariate variables. Homogeneity and normality of the dataset were checked using Levene’s and Kolmogorov–Smirnov’s tests. When required, the data were log (1 + x) transformed. A Tukey’s test was applied when significant differences were detected by ANOVA.

Community assemblage structure of meiobenthos and nematodes in the samples were compared with multivariate procedures. In detail, a similarity matrix was constructed using the Bray–Curtis measure of similarity on square root-transformed data. Non-metric Multi-Dimensional Scaling (nMDS) analysis was performed to check differences in the structure of the meiobenthic and nematode assemblages for transects and stations. The significance of these differences was tested by means of multivariate analyses of variance (PERMANOVA; Anderson 2001) on the structure of meiobenthic and nematode assemblages. The design for the analysis involved the factor Station (St; fixed, 3 levels) representative of three sampled depths, and Transect (Tr; fixed, 16 levels, nested in St) with n = 2. Post hoc pair-wise comparisons using the PERMANOVA t statistic and 4999 permutations were also carried out, if necessary. The SIMPER analysis (cut-off of 90%) was applied in order to identify the percentage contribution of each meiobenthic taxon and nematode genus to the observed value of the Bray–Curtis dissimilarity between transects and stations. All analyses were performed using the PRIMER 6 with PERMANOVA+ software package (Clarke and Gorley 2006; Anderson et al. 2008). Finally, multivariate regression analyses (DistLM; Anderson 2004) was used with step-wise selection procedure and AICc selection criterion in order to test possible significant correlations of depth and grain size with meiobenthic and nematode structures of the assemblages.

Results

Meiobenthos

A total of 17 meiobenthic taxa were identified in the study area. On average, nematodes and copepods were the dominant taxa of the meiobenthic assemblage (59 and 25%, respectively), followed by annelids (4%), ciliates (2.6%), turbellarians (2.5%), and ostracods, gastrotrichs, tardigrades (between 2 and 1.3%). All the other taxa (rotifers, kinorhynchs, amphipods, isopods, tanaids, acarids, molluscs, ascidian larvae, pycnogonids) accounted for less than 1% of the assemblage, and they were collectively named as “Others” (Online Resource 1). The highest meiobenthic taxa richness was recorded at T13 (13 taxa), while the lowest one was at T20 (3).

Total meiobenthic abundance ranged between 249.0 ± 153.5 ind. 10 cm−2 (T8) and 2189.8 ± 1193.1 ind. 10 cm−2 (T9). Shannon-diversity index showed values from 2.5 ± 0.3 (T13) to 1.2 ± 0.4 (T3 and T4), and Pielou-evenness index from 0.7 ± 0.1 (T13) to 0.4 ± 0.1 (T3, T4, T9). ANOVA revealed a significant difference between transects in the following meiobenthic parameters: taxa richness (p < 0.001), abundance (p < 0.001), Shannon (p < 0.01), and Pielou indices (p < 0.01). In detail, taxa richness appeared significantly higher at T13 especially if compared to T3, T8, T11, T16, T20 (Tukey’s test, p < 0.05). Abundance was significantly higher at T9 particularly in comparison with T1, T5, T8, T10, T13, T15, T16, T18, T19, T20 (Tukey’s test, p < 0.05). Shannon and Pielou indices resulted significantly higher at T13. The pair-wise comparisons mainly highlighted significant differences of T13 versus T3, T4, T5, T9, T18, T20 (p < 0.01) and T3, T4, T9 (p < 0.05), respectively.

ANOVA revealed also significant differences in meiobenthic taxa richness, total meiobenthic abundance, Shannon–Wiener diversity and Pielou’s evenness indices between depths. All these parameters showed a high significance level of p < 0.001 with the exception of the abundance, which resulted in p < 0.01. In detail, the deepest stations showed the lowest taxa richness (Tukey’s test, p < 0.001) along with lowest abundance (p < 0.01), and the Shannon (p < 0.001) and Pielou (p < 0.01) index values.

PERMANOVA analysis on meiobenthic assemblages showed significant differences among both transects and stations factors (pseudo-F 5.4144 and 11.367, respectively, and p < 0.001). In particular, t tests on pairwise station comparisons showed significant differences among all three depths. SIMPER routine especially documented a high level of dissimilarity of T8 and T9 followed by T20 in comparison with all the other transects (Online Resource 2). In detail, lower abundances of nematodes and copepods (adults and juveniles) were generally detected at T8, while the same transect stood out for the high abundance of tardigrades. T9 was especially marked by the high abundance of nematodes and ciliates, while T20 for copepods (mainly adults) and annelids. The comparison of depths highlighted a greater dissimilarity between coastal and deeper stations with a general decrease of all the meiobenthic taxa with depth (Online Resource 3). DistLM on meiobenthic assemblage showed that it was significantly not correlated with depth or grain-size (R 2 = 0.125 and p < 0.002 and 0.0032, respectively).

According to the ecological classification proposed by Danovaro et al. (2004) and adapted to the WFD EcoQ classes, overall the coastal area seemed to show prevalent good and secondly moderate conditions (Table 3). The meiobenthic taxa richness decreased with depth in 8 out of the 16 transects (T5, T8, T11, T12, T15, T16, T19, T20), while it was generally equivalent in 6 transects (T4, T9, T10, T13, T14, T18). The only area with a worse EcoQ in the coastal station than in the deep ones was Brindisi.
Table 3

EcoQ classification of the Apulian coasts by means of the faunal parameters of the meiobenthic and nematode assemblages (namely meiobenthic taxon richness, c-p 3 and 4 classes, Maturity Index, Shannon Diversity)

Sea sector

Stations

Meiobenthos

Nematodes

Taxon richness

EcoQ

c-p3 and 4

Maturity Index

Shannon diversity

EcoQ

Adriatic Sea

T1

14

Good

n.a.

n.a.

n.a.

n.a.

T3

11

Moderate

34

2.4

3.0

Poor

T4

14

Good

n.a.

n.a.

n.a.

n.a.

T5

13

Good

55

2.7

4.0

Moderate

T8

12

Good

n.a.

n.a.

n.a.

n.a.

T9

15

Good

32

2.4

3.4

Poor

T10

15

Good

40

2.5

3.2

Moderate

T11

12

Good

64

2.8

3.3

Moderate

T12

11

Moderate

43

2.5

3.3

Moderate

Ionian Sea

T13

14

Good

69

2.9

3.5

Good

T14

16

Good

58

2.8

3.2

Moderate

T15

14

Good

65

3.0

3.0

Good

T16

11

Moderate

64

2.8

4.0

Good

T18

14

Good

64

2.8

3.9

Good

T19

13

Good

54

2.6

3.2

Moderate

T20

11

Moderate

46

2.6

3.0

Moderate

n.a. not applicable

Nematodes

A total of 138 nematode genera were found in the study area. Xyalidae was the most abundant family (25%), followed by Chromadoridae, Comesomatidae and Desmodoridae (∼11% each). The most abundant genera were Theristus (12%) followed by Terschellingia, Epsilonema (5% each), Paramonhystera, Desmodora, Richtersia, Sabatieria, Innocuonema, Ptycholaimellus and Halalaimus (3% each).

The Shannon-diversity index ranged from 4.0 ± 0.2 (T16) to 3.0 ± 1.1 (T15), the Pielou index from 0.9 ± 0.0 (T5 and T16) to 0.7 ± 0.2 (T15), and the MI index from 3.0 ± 0.6 (T15) to 2.4 ± 0.2 (T9). The life strategy classes showed the following percentages: c-p 2 (46%), c-p3 (36%), c-p4 (17%) and c-p1 (0.04%), while c-p 5 was not detected. The c-p 3 and c-p 4 represented more than the 60% of the total nematode assemblage in T11, T13, T15, T16, T18, while colonizers (c-p 1 and c-p 2) were the dominant ones in T3, T9, T10, T12 and T20. ANOVA did not detect significant differences in the univariate nematode measures both between transects and stations. PERMANOVA analysis on nematodes assemblages showed significant differences amongamong both transects and stations factors (pseudo-F, respectively, 18.391 and 35.665 and p < 0.002); in particular, t tests on stations pairwise comparisons showed significant differences between all three depths. SIMPER highlighted generally high levels of dissimilarity (>70%) in the pair-wise comparisons, and in particular the highest dissimilarity levels (>80%) were at T15, T16, T11, T3, T13, T19, T20 (Fig. 3, Online Resources 4, 5).
Fig. 3

Non metric Multi-dimensional Scaling plot of the nematode assemblages (stress level: 0.20): a compared between the various transects, b between depths (stations), and indicated by the respective labels

DistLM on nematodes assemblages showed that they were not significantly correlated with depth or grain-size (R 2 = 0.114 and p < 0.002 and 0.002, respectively).

Shannon-diversity showed mainly a moderate EcoQ (T3, T9–12, T14, T15, T19, T20) and secondly a good one (T5, T13, T16, T18) (Table 3). MI revealed a heterogeneous situation with an EcoQ from poor (T3, T9) to high (T13). The EcoQ more frequently detected was good (T5, T11, T16, T18, T20), followed by a moderate value (T10, T12, T19). The classes of life strategies showed a prevalence of moderate (T5, T10, T12, T14, T19, T20) and good values (T11, T13, T15, T16, T18), followed by poor (T3, T9) EcoQ values. When the overall EcoQ of the coastal stations was assessed using the three nematode descriptors, the worst quality was revealed at T3, T9, while the best one at T13, T15, T16 and T18 (Table 3). When the EcoQ was evaluated along the depth gradient, it generally appeared comparable in transects T12, T13, T15, T16, T18, T19 and T20. Conversely, T3, T9, T10 and T14 showed lower values of the nematode faunal indicators at the coastal stations, while T5 and T11 at the deep stations.

Discussion

Data available on the meiobenthic and nematode assemblages of the southern Adriatic and northern Ionian sectors are mainly focused on the subtidal zone, but they are still few and patchy distributed (e.g. Sandulli et al. 2004, 2010, 2014; De Leonardis et al. 2008).

The total meiobenthic abundance recorded in the present study appeared higher than that previously recorded along the Apulian coasts (Sandulli et al. 2004; De Leonardis et al. 2008). However, the levels of taxa richness and biodiversity of the meiobenthic assemblage were higher than in previous studies (e.g. De Leonardis et al. 2008; Sandulli et al. 2010). As reported by Sandulli et al. (2010), ciliates were also documented in this survey. Protozoans are not commonly included in the ecological surveys, but, as underlined by Giere (2009), the ecological picture of a marine ecosystem cannot be drawn without considering benthic protists.

ANOVA revealed significant differences of meiobenthic univariate parameters between both transects and depths (i.e. meiobenthic taxa richness, total meiobenthic abundance, Shannon–Wiener diversity and Pielou’s evenness indices). In detail, meiobenthic taxa richness and Shannon and Pielou indices appeared significantly high at the Galliano area (T13), characterized by a low human impact, while total meiobenthic abundances were higher at Torre Specchia (T9) due to a high contribution of nematodes and ciliates. ANOVA showed significant low values of all the meiobenthic univariate measures along the depth gradient. Also nMDS revealed the dissimilarity between depths, confirming a progressive abundance decrease of all the faunal groups at the stations T3. These decreasing trends produced significantly different meiobenthic assemblages at all depths as highlighted by PERMANOVA. Indeed, the reduction of the interstitial spaces in the sediments leads to a decline of the meiobenthos due to a loss of trophic niches and a dominance of few and tolerant infaunal organisms, namely nematodes (Vanaverbeke et al. 2002; Balsamo et al. 2010; Semprucci et al. 2011, 2013b). However, the literature about the trends of the meiobenthic abundance is not univocal. Some authors noticed an inverse relationship between abundance and depth, as in our study (Tietjen 1992; Vincx et al. 1994; De Leonardis et al. 2008), whereas others found a positive correlation (Semprucci et al. 2010a, 2015b). In this investigation, using DistLM, no correlation was found between meiobenthic assemblages and the considered environmental factors (depths and sediment grain size), showing that an external factor might be responsible in forcing the assemblage structure such as human impact.

Both WFD and MSFD state that the European countries should develop monitoring programs for evaluating system health and hence allowing a confident assessment of GEnS (Van Hoey et al. 2010). In the present study, when the EcoQ thresholds suggested for meiobenthos were applied, the study area seemed to fall in a prevalent good EcoQ class followed by a moderate one (Pusceddu et al. 2007). The EcoQ detected by the meiobenthic composition seems to highlight the low EcoQ conditions at Brindisi (T3) and Castro (T12) which are a harbour and a mussel farm infrastructure, respectively. However, a moderate EcoQ was also revealed at Porto Cesareo (T20) notwithstanding the presence of a MPA that was subject to an overload of tourism and infrastructure building in the past years (CoNISMa 2001). Comparing the EcoQ along the depth gradient, the lower values at the coastal area only at the Brindisi transect appeared due to the high level of disturbance of the harbour.

As for the meiobenthos, the nematode assemblage appeared rich and generally well diversified with diversity levels higher than in the previous studies (De Leonardis et al. 2008; Sandulli et al. 2010). The most abundant nematode genera are known to be associated with muddy sediments (Semprucci et al. 2013b, 2014) with the only exception of Epsilonema, which is generally recognized as an epifaunal genus of coarse sediments (Raes and Vanreusel 2006; Raes et al. 2007). Transects showing the highest dissimilarity (SIMPER test) were T20, T19 (Porto Cesareo MPA and S. Isidoro) and T3 (Brindisi Harbour). All of them were distinguished by the high abundance of the genus Terschellingia (family Linhomoidae), followed by the genera Sabatieria and Setosabatieria (fam. Comesomatidae) and Theristus (fam. Xyalidae). All these taxa are known as mud-dwelling nematodes (De Leonardis et al. 2008; Vanreusel et al. 2010; Sandulli et al. 2014), but they are also linked to environmental disturbances such as sewage discharges, fish-farm cages, trace elements and hydrocarbons (Balsamo et al. 2012; Semprucci et al. 2015b; Zeppilli et al. 2015). The environmental disturbance seems to be the most probable hypothesis to explain the dominance of these genera in the three transects which cannot be explained by granulometry. Taxa typical of coarse textures such as Epsilonema and Dracognomus (Gourbault and Decraemer 1994; Raes and Vanreusel 2006; Semprucci et al. 2010b) characterized T13 (Gagliano) and T15 (Torre Mozza), both with coarse sediments. Desmoscolex (Desmoscolecidae) is generally considered a sensitive taxon (e.g. Moreno et al. 2011), and it allowed the discrimination of T13 (Gagliano) and T16 (S. Giovanni-Mancaversa), two areas characterized by low human impact and quite heterogeneous sediments. The species of Desmoscolex frequently inhabit muddy and deep sediments (Vanaverbeke et al. 1997; Soetaert et al. 2002), but they are also found in association with biogenic fragments (Vanreusel et al. 2010; Semprucci et al. 2013b, 2014). Thus, this genus was defined as a sediment-dwelling taxon by Raes and Vanreusel (2006), who underlined its frequency in a large variety of substrata.

However, nematode structure did not seem directly related to grain size variations, as highlighted by DistLM analysis, but rather to the environmental disturbances. As previously reported for Adriatic Sea, c-p 2 and c-p3 were the prevalent nematode life strategies (Semprucci et al. 2010a, 2015a). When EcoQ was assessed using the thresholds of nematodes (Moreno et al. 2011; Semprucci et al. 2014), the worst quality was detected at T3, T9 and T10. The ecological conditions revealed by the meiobenthic and nematode assemblages seemed to be generally consistent and the higher human impact appeared at Brindisi harbour. The only exception to the compared results of the two benthic assemblages was at Torre Specchia (T9), in which meiobenthos highlighted a high richness of meiobenthic taxa and thus a good EcoQ, whereas nematode parameters revealed a poor EcoQ. Taxa richness is the tool currently used for the EcoQ classification of the marine ecosystems using meiofauna (e.g. Pusceddu et al. 2007; Semprucci et al. 2015a; Bianchelli et al. 2016). However, it should be noted that it measures only the number of taxa detected in the samples and not the overall possible contribution of opportunistic taxa (Semprucci et al. 2016). In this respect, T9 revealed a strong dominance of nematodes. The EcoQ of the sediment generally appeared similar along the depth gradient, but T3, T9 and T10 showed lower values of the nematode faunal indicators at the coastal stations, confirming a possible greater human influence in these localities.

Overall, the Adriatic area seems to be more affected by the anthropogenic activities than the Ionian ones, as confirmed by the PERMANOVA results, and it underlines the importance of further monitoring studies to integrate the present data and evaluate possible variations of the ecological quality of the Apulian coast over time.

Notes

Acknowledgements

The study was financially supported by the CoNISMa, project: “Interreg Italia/Grecia (Rete di gestione delle acque della regione meridionale del Mare Adriatico e del Mar Ionio – Tutela Ambiente Marino)”. We are grateful to the staff of the Department of Zoology (University of Bari) for their help during the sample analysis. We warmly thank the anonymous reviewers, and the Scientific Editor Dr. Daniela Zeppilli for their helpful comments that have greatly improved the manuscript.

Supplementary material

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Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Federica Semprucci
    • 1
  • Maria Balsamo
    • 1
  • Luca Appolloni
    • 2
  • Roberto Sandulli
    • 2
  1. 1.Dipartimento di Scienze Biomolecolari (DiSB)University of UrbinoUrbinoItaly
  2. 2.Dipartimento di Scienze e Tecnologie (DiST), CoNISMaUniversity of Napoli “Parthenope”NaplesItaly

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