ELSEVIER
MarineGeology 122(1995)367-384
150 years of eutrophication in the northern Adriatic Sea: Evidence from a benthic foraminiferal record D.M. Barmawidjaja a, G.J. van der Zwaan bv*,F.J. Jorissen ‘, S. Puskaric d a Marine Geological Institute, Jalan Dr. Junjunan 236, Bandung 40174, Indonesia b Institute of Earth Sciences, University of Utrecht, Budapestlaan 4, 3584 CD Utrecht, The Netherlands ’ University of Bordeaux, Department of Geology and Oceanography, Avenue des Facultt?s, 33405 Talence cedex, France d Institut Ruder Boskovic, Center for Marine Research, 52210 Rovinj, Croatia Received 7 June 1994; revision accepted 22 November 1994
Abstract
The vertical distribution of benthic foraminifera in a sediment core in front of the PO delta has been studied in detail. According to our age model, based on 210Pb and 137Csanalyses of another core from exactly the same locality, the studied core spans the past 160 years. The radio-isotope profiles further show that sediment mixing is largely restricted to the top centimeter, suggesting that the core should provide an extremely detailed record of the youngest history of the northern Adriatic Sea. Benthic foraminiferal patterns and grain-size analyses indicate a number of substantial changes in sedimentation rate and food/oxygen availability in the benthic ecosystem. Changes occurring at about 1840 and 1880 can be attributed to man-induced changes in the main outflow canals of the PO river. The first one led to an important reduction of the marine vegetation cover which probably was present up to that date. The second change resulted in the present-day situation in which the PO outflow is passing the studied core locality close by. The local benthic foraminiferal associations indicate a steadily increasing nutrient load from 1900 AD onwards. This trend is interpreted as the effect of anthropogenic eutrophication due to agriculture and waste water disposal, although the fauna1 record as discussed here only gives a limited impression of the basin-wide development. A marked faunal transition around 1930 indicates intensification of the eutrophication; around 1960 the first signs of an increasing importance of anoxic events can be recognized. The fauna1 changes in the last decade, which are ascribed to changes in preservation potential, indicate that more intense or more prolonged anoxia started about 10 years ago, and that the ecological health of this part of the northern Adriatic probably is still in decline.
1. Introduction The influence of the river PO as the main eutrophication source of the northern Adriatic Sea is beyond dispute. The enormous input of fine-
Concurrently, large quantities of nutrients are brought into the basin, leading to high primary production. In late summer and autumn, the combination of thermal stratification and a high downward organic flux leads to dysoxic, or even anoxic,
grained matter by the PO river and the subsequent transport by surface currents, has resulted in a well-defined clay belt along the Italian coast.
bottom water conditions over an increasingly large area (Giordani and Angiolini, 1983; Chiaudani et al., 1983; Justic, 1987; Marchetti et al., 1988; Degobbis, 1989). The effects of these bottom water
* Corresponding author.
conditions
0025-3227/95/%09.50 0 1995Elsevier Science B.V. All rights reserved SSDI 0025-3227(94)00121-9
on the benthic
foraminiferal
distribu-
368
D.M. Barmawidjaa et al./Marine Geology 122 (1995) 367-384
tion patterns have been described by Jorissen (1987, 1988) Van der Zwaan and Jorissen (1991), Jorissen et al. (1992) and Barmawidjaja et al. (1992). The records of the PO river nutrient load (Marchetti et al., 1989), sea water transparency (Justic, 1988), and anoxic events of the past decades (Justic et al., 1987) all suggest that the anthropogenic nutrient input is increasingly affecting the marine environment. We have virtually no knowledge as to the change from the past “natural” fluviatile-marine interaction, to the presentday strongly human-influenced situation. In a recent paper, Puskaric et al. (1990) described a strong and sudden increase of phytoplankton over the past 40 years. This was taken as a sign of the strong post-war increase of phosphorous, originating from human activities. Especially the increase of coccolithophorids would be indicative for this increase in nutrient discharge. They considered the increase of siliceous remains to reflect the decrease of oxygen concentrations in the bottom environments over the past decades. In the present paper, we will attempt to document the eutrophication history over a considerable period of time. To this end, we analyzed the benthic foraminifera preserved in a core in close detail; we had a reliable time control for the last 70 years, and we expected (on the basis of linear extrapolation) to document the past 160 years, i.e. the period from about 1830 to 1990.
2. Material and methods In July 1990, a 57 cm long sediment core was taken by SCUBA divers using a portable PVC coring device at station 108 (Fig. 1), at a water depth of 32 m. Samples taken earlier at the same station are discussed extensively by Puskaric et al. (1990) Jorissen et al. (1992) and Barmawidjaja et al. (1992). Fig. 1 shows that the substrate at this station, which is located in front of the PO delta, is predominantly muddy. The effect of the PO outflow on the sedimentation pattern is clearly reflected by the rather narrow, but well-defined, mud belt which has developed in southward direction along the Italian coast.
45O30’
49
44030
44"
Fig. 1. Location of sample station 108 (44”45.4’N, 12”45.O’E, water depth 32 m), together with a simplified surface sediment map (after Brambati et al., 1983). Stippled area indicates active clay deposition.
Puskaric et al. (1990), who in 1989 collected a 110 cm long core at the same station, noticed an upward transition from sandy pelite to pelite at 60 cm depth, slightly deeper than the bottom of our core. In order to demonstrate a possible finingupward trend, and to search for other variations in grain size, detailed grain-size analyses were performed on 12 evenly spaced samples. For these analyses we employed a Laser Particle Sizer, and followed standard routines. The core was sliced in l-cm intervals. The samples were washed carefully over a set of sieves; for this study the 63-595 urn size fraction has been employed. We studied all samples in the upper 30 cm, whereas 16 samples were studied in the lower 27 cm of the core; in all 46 samples were
D. M. Bannawidjaja et al./Marine Geology I22 (1995) 367-384
studied. For all samples complete splits were used until a minimum number of 300 benthic foraminifera had been picked, determined, and counted. For the determination of foraminifera we followed the taxonomy of Jorissen (1987, 1988) and Barmawidjaja et al. (1992).
3. Age model In a study of a core taken in 1989 at the same sample station, Puskaric et al. (1990) employed two isotopes with a different origin and half-life time: 13’Cs (t1,2=30 yr) and ‘l”Pb (t,,,=22.4 yr). There are two different sources of caesium. The first one is the fallout of nuclear bomb explosions. The first year of significant i3’Cs fallout was 1954, whereas this isotope reached a peak value in 1963. This last maximum was recognized by Puskaric et al. (1990) at a depth of 7.5 cm, which thus would coincide with an age of 26 years (Fig. 2). 210Pb
excess
(dpm/g)
of station
108
10
O'O 4 -z-8 212 5 16 0 -0 20
. .
24 28
I:::::.
137Cs
(Bq/kg)
0 2
0.2 -134
at station 0.4
108
0.6
CS
369
The second source of caesium is the fallout produced by the Chernobyl nuclear power plant accident in April 1986. This second event coincides with a peak value of 134Cs, which, in the light of its very short half-life (t1,2= 1.9 yr), can only be related to the 1986 Chernobyl accident. Puskaric et al. found this isotope only in the topmost centimeter (Fig. 2), indicating that the top of the core was intact, but also, that deep bioturbation is minimal. The average sedimentation rate resulting from the 1963 peak is 0.35 cm/yr. Exactly the same result was arrived at by employing the profile of ‘l”Pb in the top 20 cm of the core (Fig. 2), corresponding with the interval from 1919 to 1989. It is important to note that also the 210Pb-profile suggests that the maximal thickness of the sediment surface mixed layer is one cm, indicating a nearabsence of larger deep-burrowing organisms. Since our core was taken at exactly the same location as the one studied by Puskaric et al. (1990), we assume that the age model they arrived at is also applicable to the top 20 cm of our core. By a downward extrapolation of the sedimentation rate of 0.35 cm/year we would obtain an age of about 160 years for our bottom sample (56-57 cm below the core-top). If the thickness of the sediment mixed layer in the past has been just as thin as it is at present, mixture of sediments by bioturbation has been minimal. Therefore, our core could document the development between 1830 and 1990 in great detail. However, we have to admit that the age constraints are much looser in the lower part than in the top part of the core, and that, in case the bottom environment was better oxygenated, the thickness of the surface mixed layer could have been greater in the past.
4 Y6 .%a
-1963
510 E 012 14 16 18 -1-;
Fig. 2. ‘lOPb, 13’Cs and 13%s profiles of a sediment core sampled at station 108 in 1989 (after Puskaric et al., 1990). For discussion see text.
4. Grain-size analyses We analyzed 12 samples on grain-size distribution patterns in order to check whether there are significant changes over the cored interval. For each sample multiple (5-8) analyses were performed in order to assess analytical variability. The average values of all reliable runs are depicted in Fig. 3. The results indicate a remarkable constancy in grain-size distribution. Two features
D.M. Barmawidjaja et al./Marine Geology 122 (1995) 367-384
370
0-lcm
4-5cm
9-10cm
14-15cm
19-ZOcm
24-25~1
29-30cm
34-35cm
39-4Ocm
10%
44-45cm
49-5Ocm
54-55cm
0
Fig. 3. Grain-size distribution patterns (in micrometers) in 12 samples; in each case the curve depicts the average values of 5 to 8 reliable runs.
stand out: from the 34-35 cm sample until the 9-10 cm sample a clear shoulder can be noticed in the 3.0-3.8 pm grain-size class; secondly, the curves from the two lowermost samples (49-50 cm and 54-55 cm) display a rather distinct shoulder in the larger grain-size classes (13.0-53.5 pm). It is difficult to assess whether this latter feature, the secondary peak in the larger grain-size classes, is real or an artefact caused by flocculation of clay particles. As it is, a preliminary conclusion could be that the two lowermost samples are somewhat coarser than the other samples. However, the mean values of all 12 samples are remarkably close. The impression of homogeneity is confirmed by an ANOVA (two-way analysis of variance, checking differences between samples over all size classes by means of F-test; see Davis, 1988) carried out for all 12 samples and for subsets of samples in various combinations. According to these statistical analy-
ses the probability that samples belong to different populations is less than 1% (P~0.01). This confirms our visual impression that there is little difference between the samples and that there is no dramatic break in the sedimentation pattern.
5. Fauna1 patterns The counting results of the 59 taxa recognized are listed in Table 1. In Fig. 4b relative abundances of the 28 most frequent taxa are presented versus core depth and absolute age. The most remarkable feature in the total number (per standard volume of sediment) curve (Fig. 4a) is the clear break at about 50 cm depth. Below this level much higher total numbers are found than above it. A second break, although of smaller magnitude, occurs around the 40 cm level. This pattern could have
_
E:
#ample that has been counted
9
IO
II 6 8 12 6 I 4 8 10 9 2 4
IX 9 16 8 6 7 16 10 12 12 5 6 0 3 8 8 9 2 5 2 IO 3 3 3 7 4 6 5 2 3
I 5 IO 3 6 10 5 4 19 6 8 5 6 6 5 6 8 3 5 7 5 4 4 4 8 I 2 2 0 3 2 2 4
I
I I I 2 0 3 I I I 0 I 0 0 I 3 0
II I 3 2 4 9 2 2 0 4 5 2 I I 0 4 I I 1 I 2 3 3 2 2 3 4 2 2 2 4 2 2 2 2 2 I 0 0 0 2 0 0 I 0 0 3
(8 = l/S of the total sample, etc.). Numbers
1 to 60 indicate
the vario
12
13
14
15
16
17
18
19
20
21
28 IO 12 12 6 6 IO 5 12 9 7 I 2 3 11 II 5 5 3 I 21 2 0 0
34 25 12 12 I4 10 I4 14 17 14 10 17 0 15 24 15 II 7 22 9 25 9 8 I4 5 5 11 10 IO 9 4 4 13 8 2 6 9 IO 7 7 7 5 8 7 5 7
0
0
0
0
54 24 42 24 28 15 28 16 37 47 I1 29 I 23 56 49 25 24 39 40 86 39 42 41 39 31 29 31 38 41 31 30 39 35 22 24 39 44 17 10 16 5 5 II 8 7
0
2 3 0 0 0 3 4 0 1 0 2 7 1 3 2 0 1 I 3 5 0 2 2 3 1 2 1 0 3 I 2 6 7 2 0 8 8 6 6 3 6 IO IO 6 9
0
0
1
0
1
0
0
0
8 5 1 2 3 2 6
1 5 0 2 4 1 1 I 1 1 2 I 69 0 6 0
2 3 4 3 0 0 1 I 3 2 0 2 16 2 3 2 5 0 0 3 2
I 3 0 2 I I 0 0 I 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 1 0 0 0
1 0 0 0 1 0 0 0 0 0 0 I 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0
0
1
0
2 0 0 0 2 1 0 0 1 1 2 1 1 0 0 0 0 0 0 0 0 0 0 I I 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
0 0
0 0
I 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
I 9 2 3 4 2 3 9 6 2 0 5 1 5 4 3 2 7 I 3 5 4 4 4 5 2 4 0 3 5 0 2 3 3 I 3 5 0 4
1 4 0 0 1 0 0 0 1 0 0 1 1 3 2 2 0 1 0 1 I 0 1 0 0 0 0 2 4 1
1 3 0 3 5 1 0 0 2 2 2 5 5 3 3 6 2 3 8 3 5 7 9 7 21
22 3 8 2 0 I 5 7 I I 3 4 3 2 0 2 2 0 0 0 1 7 I 0 3 1 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
‘s praegeri; 2 Ammonia beccarii; 32 = Hanrawaia boueana; 3 = Ammonia parkinsoniana; 33 = Haplophr ivina dilatata. typical-type; 40 = Nonionella turgida; 1I = Bolivina pseudoplicata; 41 = Polymorphinidae ella sp.; 48 = Quinyueloculina stalkeri; 19 = Cassidulina crassa; 49 = Reophax nana; 20 = Cassidulina ms; 27 = Elphidium poeyanum; 57 = Tr@rina angulosa pauperara; 28 = Elphidium sp. 1; 58 = Triloculin
D. M. Barmawidjaja et aLlMarine Geology I22 ( I
60 indicate
the various
taxa counted.
20
21
22
23
24
25
26
27
28
29
30
31
1
2 4 1
2 3 4 3 0 0
I I
1
3 2 0 2 16 2 3 2 5 0 0 3 2
9 7 6 2 4 2 2 5 5 II 3 5 2 7 12 3 4 12 0 4 8 5 8 5 9 4 7 6 4 I 6 5 4 2
8 6 5 6 8 1 4 4 6 3 2 2 0 2 4 3 2 3
2 1 5 1 0 0 1 I 0 2 2 1
18 11 I5 13 I 8 16 11 11 15 9 8 8 10 21 15 8 8 12 8 22 17 19 17 16 17 31 22 17 25 24 12 21 32 23 8 12 27 18 11 23 14 26 9 27 24
39 16 30 17 12 7 16 22 16 13 11 8 9 13 19 20 12 I 32 11 45 18 31 25 24 43 30 27 28 31 36 23 27 38 46 29 43 42 23 19 29 27 19 33 36 26
33 31 34 20 15 23 26 26 23 22 11 30 18 16 27 30 24 14 30 21 76 16 21 53 29 39 43 28 43 50 55 44 33 53 58 64 43 41 41 55 68 83 16 19 92 102
53 35 35 41 24 23 25 31 49 54 24 41 12 23 50 48 31 26 42 31 114 43 43 49 52 40 38 59 43 56 39 53 62 54 27 28 33 23 40 29 14 20 16 22 18 33
4 1 2 4 4 2 3 3 7 7 1 1 4 0 10 2 0 4 0 3 10 3 2 2 0 3 4 4 2 4 1 4 2 4 0 3 2 1 1 4 3 3 2 3 1 2
I 2 3 0 1
I I
3 8 2 0 1 5 7
5 0
1 2 1 69 0 6 0 I 4 0 0 1 0 0 0 I 0 0 1
I 3 2 2 0 1 0 1 1 0 1 0 0 0 0 2 4 1
I 1 3 4 3 2 0 2 2 0 0 0 1 1
I
I
3 0 ,
0
; 1 0 0 2 2 2 5 5 3 3 6 2 3 8 3 5 7 9 7 21
1 0 0 0 0 I 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
3
1
I 3 0 2 2 2 0 3 0 0 0 0
1 3 6 3 2 5 5 4 4
1 2 0 2 0 2 5 8 1
I 10 3 2 4 12 3 11 11 17
I 2 3 1 0 2 2 2 2 5 1 2 4 4 5 2 2 3 4 3 6 3 5 3 3 5 0 0 1 4 0 0 1 2
I 1 2 2 2 2 4 0 2 4 2 1 1 5 2 7 0 2 3 3
1 3 5 2 2 5 5 5 6 5 3 3 5 12 4 12 12 5 16 10 17
32
33 2 1 3 3 0 2 2
1 5 1 1 0 4 0 3 0 0 1 0 2 5 I 0 0 I 0 0 1 1 0 3 0 0 2 2 0 0 0 3 0 0 0 0 2 0 0
lsoniana; 33 = Haplophragmoides kosterensis; 4= Ammonia perlucida; 34 = Hopkinsina pacifica; 5 = An ; 41= Polymorphinidae spp.; 12 = Bolivina seminuda; 42 = Pseudoeponides falsobeccarii; 13 = Bolivina . rana; 20 = Cussidulina subglobosa; 50 = Reussella spinulosa; 21= Cibides lobatulus; 51= Rosalina spy m sp. 1; 58 = Triloculina tricarinata; 29 = Epistominella exigua; 59 = Triloculina trigonula; 30 = Fissure
31 1 2 3 0 1 I 1 2 2 2 2 4 0 2 4 2 1 1 5 2 7 0 2 3 3 1 3 5 2 2 5 5 5 6 5 3 3 5 12 4 12 12 5 16 IO 17
32
33
34
35
36
37
38
I
2 1 3 3 0 2 2 I 5 7 I 0 4 0 3 0 0 1 0 2 5 I 0 0 1 0 0 I I 0 3 0 0 2 2 0 0 0 3 0 0 0 0 2 0 0
3 21 36 39 32 18 24 23 19 30 7 11 6 1 24 IO 6 7 15 9 27 2 1 I 5 0 3 3 3 I 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
I
4 0 0 2 3 3 4 0 2 0 0 I 0 6 2 I 0 0 0 2 0 1 2 I 0 3 1 1 0 0 0 1 0 0 0 0 0 0 0 0 0 2 I 1 1
13 15 2 3 I 2 2 1 1 4 I 0 1 0 I 1 0 0 0 I 0 0 2 0 0 2 2 0 4 2 2 1 5 5 2 6 4 2 0 4 2 4 0 3 I 0
9 1 6 9 5 7 0 II 15 12 7 9 2 4 10 3 2 2 6 6 5 5 1 I 1 3 2 3 3 3 2 2 2 4 2 2 0 0 0 0 2 0 0 0 0 0
0 0
I 0
0 0 0 0
0 0 0 0 0
0 0
0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 I 0 I 0 0 0 0 0 I I
-
39
40
41
42
43
0
5
0 2 0 0 2 0 5 2 0 0 7 0 1 I 0 0 0
179 101 118 152 159 141 170 173 I84 154 83 101 95 76 238 170 126 101 148 98 292 96 84 110 112 66 62 89 84 67 80 60 61 59 42 29 34 36 19 30 28 28 26 35 24 28
2 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 I 1 I 0 0 0 I 0 0 2 0 0 0 0 0
6 9 3
0
0
I
0
4 3 7 5 1 5
0
2 1 0 0 0 0 1 1 2 0 1 0 0 0 1 0 3 0 0 0 2 0 0 2 4 0 2 1 3 0 0 2 I 2 4 4 1 3 2 9 5 1 6 8
1 0 5
1 0 2 0 0
1 1 I 0 I 1 3 4 4 0 0 1 I 6 4 4 7 8 5 3
1 I 0 1 0 0 0 0 0 0 0 1 0 0 0
0 0
0 0 0 0 0
I
0
3 3 3 4 5 4 3 9 7 13 4 2 IO 9 5 7 6 5 IO 5 4 7 3 6 13 6 6 10 6 7 3 2 4 1 2
0
0 0
1 0 0 0 0 0 0 5 0 0 2 0 0 0 1 0 0 0 2 0 0 0 1 2 1 1 0 0 0 0 0 1
wina pacijicu; 5 = Ammoscalaria pseudospiralis; 35 = Lagmu spp.; 6 = Amphicoryna scalar ccarii; 13 .= fiolivina sputhulata; 43 = Pvrgo suhsphaerica; 14 = Buccella gramdata; 44= Qu, u; 51 = Rosa&a spp.; 22 = Eggerella advena; 52 = Sigmoilina distorta; 23 = Eggerella so rigonula; 30=Fissurina spp.; and 60=spec.indet.
42 6 9 3 1 4 3 7 5 1 5 1 3 3 3 4 5 4 3 9 7 13 4 2 10 9 5 7 6 5 10 5 4 1 3 6 13 6 6 IO 6 7 3 2 4 I 2
43
44
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
1 0 0 0 2 0 0 0 1 0 I 3 0 2 0 I I 2 1 0 I 0 2 2 0 2 3 0 I 0 0 0 0 0 0 0
0 0 0
1 0 0 0 0 0 0
5 0 0 2 0 0 0 1 0 0 0 2 0 0 0 1 2 1 1 0 0 0 0 0 1
45 4 3 5 0 I 0 2 0 0 0 3 0 4 0 1 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 I I 0 I 0 0 1 0
46 12 17 I1 IO 2 7 I 4 5 9 4 5 1 1 5 5 5 6 2 7 14 2 7 13 20 15 11 15 7 15 16 5 10 7 9 8 II 12 5 4 2 3 0 2 2 4
47 5 5 7 4 2 0 4 0 2 3 I 1 2 2 I 1 1 I 0 0 0 2 0 1 0 0 5 5 0 I 0 0 2 I 1 0 0 2 0 0 1 4 0 2 4 6
48
49
50
51
52
53
54
23 32 30 33 39 22 35 26 26 35 5 17 18 13 37 30 19 16 20 18 22 2 3 2 0 8 2 0 11 3 8 5 2 6 4 0 2 0 0 2 0 0 0 0 1 0
0
I
0
0
I1 13 1 6 3 5 2 3 12 3 4 4 0 0 0 0 0 3 2 2 0 1 1 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0
4 3 2 2 0 2 5 1 2 3 2 2 2 5 2 0 0 2 1 5 0 1 3 0 3 1 2 0 6 3 2 1 2 5 8 2 8 2 1 6 7 2 7 12 8
0
0
3 2
0
2 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 2 0 2 0 0 1 I 0 2 0 0 2 2 0 2 1 0 3 I 0 1 0 2 1 2 1 1 0
3 2 I 2 0 2 1 2 2 5 I 2 IO 8 2 I 7 3 9 6 1 3 7 4 6 6 5 6 3 4 6 6 3 2 3 4 2 4 I 0 0 I 2 0
12 6 12 6 3 2 2 7 6 3 2 4 2 2 1 0 I 2 5 1 4 I 0 1 1 0 1 2 0 0 0 I 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0
0 0 0 0 0 0
1
1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 I 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0
;coryna scalaris; 36= Miolinella SQQ.;7 = Asterigerinara adriaticu; 37 = A4orulueplectu bulbos data; 44 = Quinqueloculinu hadenensis; 15= Bulimina costata; 45 = Quinqueloculinu oblonga; Eggerella scabra; 53 = Sigmoilopsis schlumbergeri; 24 = Elphidium udvenum; 54 = StuinfbrtA
I
pp.371-376
53
54
55
56
57
58
59
60
Total
3 2 3 2
12 6 12 6 3 2 2 I 6 3 2 4 2 2 I 0 I 2 5 1 4 I 0 I 1 0 I 2 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0
13
9 15 15 9 15 3 II 4 II 18 6 10 7 9 33 21 12 9 16 7 30 14 12 18 24 21 IS 13 13 21 26 21 19 2s 17 13 14 30 15 IX 23 29 I6 27 22 20
0
0 1
0
0
0
0
0
0
0
I
0
0
0
0
2
0
4
0
0
I
0
3 4 3 0
0
I I 2 2 3
0
1 0 0 0 0 0 0 0 I 0 4 0 3 I 0 0 0 0 I 5 2 0 2
663 493 559 496 453 371 484 414 552 576 263 377 269 270 709 529 354 302 471 357 969 360 351 449 453 398 390 392 384 430 420 346 445 464 395 312 336 395 298 303 338 312 322 396 400 443
I 2 0 2 1 2 2 5 1 2 IO 8 2 1 I 3 9 6 1 3 7 4 6 6 5 6 3 4 6 6 3 2 3 4 2 4 I 0 0 1 2 0
kwpkctu hulhosu;
4 14 7 4 8 5 9 11 I 2 0 0 2 I 2 1 0 5 2 7 3 5 4 5 3 2 2 2 2 3 3 3 2 3 2 I 0 2 I 2 0 I 0 I I
54 = Stainforthiu
_/is@-mis.
0 0 0
1 0 1 2 0 0 0 0 0 0 0 0 0 I 0 0 0 0 I 0 0 I 0 0 0 0 I 0 0 0 0 0 0 0
6
I 3 3 4 I 0 3 5 3 0
I 2 2 2 1 2 3 3 1 0 3 4 2 2
I I I I 5
8= Asterigrrinufu
culinu ohlongu; 16 = Buliminu
;
I 1 2
mumillu;
murginutu;
f.1; 25 =
I 4 2 I 0 I 3 2 0 I 0 0 1 0 0
I 2
I
0 0 0
I
1 0 0 0 I 0 0 0 0 0 0 2 0 I I I 0 0 I 0 I 0 I I 0 0 0 0 I I 0 1 I 0 0 0
Taxon Split 8 8 8 8 8 8 8 8 8 8 16 16 I6 16 8 8 16 16 16 16 8 16 16 I6 16 8 16 16 16 I6 16 16 16 16 16 32 32 32 32 32 32 32 64 64 128 64
38 Neoconorhinu teryuemi; 9 =
46 = Quinyurloculinu Elphidium
seminulu; 17 =
crispurn; 55 = Stuinfbrthiu
D. M. Barmawidjaja et al./Marine Geology 122 (1995) 367-384
TOTAL
FAUNA
317
(4 P
0
1990
10 1950
20
30
40
50
(b)
P - 1990
- 1950
-1900
-1850
Fig. 4. (a) Numbers of benthic foraminifera per standard volume (38.5 cm3) sediment. (b) Relative abundances (percentages of total benthic foraminiferal fauna) of the 28 most frequent taxa.
378
D.M. Barmawidjaja et al. JMarine Geology 122 (1995) 367-384
two causes; a substantial lowering of benthic production and/or an increase in sedimentation rate. In this respect it is worthwhile to recall that the lowermost two samples studied on grain-size patterns indeed suggest a somewhat coarser substrate, which could be indicative of a smaller input of PO-derived muds. The changes in fauna1 composition coinciding with these foraminiferal accumulation rate patterns are much more gradual. Basically a fauna dominated by Elphidium spp. and Asterigerinata adriatica is, by a number of steps, eventually replaced by a fauna dominated by Nonionella turgida (Fig. 4b). The gradual disappearance of a number taxa with a planoconvex morphology, which is typical for epiphytic taxa (Asterigerinata mamilla, Buccella granulata, Cibicides lobatulus, Gavelinopsis praegeri, Neoconorbina terquemi), and the
concurrent increase in relative abundance of muddwellers (e.g. Ammonia perlucida, Bulimina marginata, Epistominella vitrea) suggests that a vegetation cover rather gradually disappeared, although the species are not diagnostic for the type of vegetation involved. Simultaneously, the substrate became somewhat better sorted, lacking the coarser grain-size classes. This suggests that the most feasible explanation for the two drops in total numbers in the basal part of the core is not a decrease in production, but an increase in sedimentation rate in a predominantly muddy setting, leading to an almost complete destruction of vegetation. Foraminiferal accumulation rates are rather stable in the top part of the core, suggesting a constant sedimentation rate. This is supported by the constancy of the grain-size patterns and by the tight age model constraining the top 20 cm. Therefore, the strong decrease in river sediment supply over the past few decades, observed by Dal Cin (1983) and Dal Cin and Simeoni (1987), apparently did not lead to a significantly lower sedimentation rate at our sample station. After the fauna1 turnover in the basal part of the core, a very gradual, long-term trend can be distinguished in the mud-dwelling association in the higher part of the core (Fig. 4b). Nonionella turgida and a number of correlated taxa increase in (relative) frequency; until about 20 cm at the expense of species as Ammonia perlucida, Elphidium
granosum,
Elphidium poeyanum
and Elphidium at the expense of Bulimina marginata, Epistominella vitrea and Pseudoeponides falsobeccarii (Fig. 4b). A cluster analysis confirms the four-fold division of our fauna1 associations (Fig. 5). A first cluster is numerically dominated by N. turgida, a second cluster by B. marginata and E. vitrea. A third cluster consists of two subclusters: the first one, which contains a number of epiphytes, is numerically dominated by Elphidium spp., and the second one is made up by A, perlucida, E, granosum and SPPY and thereafter
E. poeyanum.
The temporal pattern of the faunas is easily identified by a Principal Component Analysis. The plot of scores on the first two (significant) principal component axes (Fig. 6) shows that the first axis is almost exclusively loaded by N. turgida (positively) and by Elphidium spp. (negatively). The main, rather gradual, turnover takes place between 40 and 20 cm. At the 20 cm level, Hopkinsina paczjica and other species of cluster 1 enter the record or become more frequent; here the scores on the first factor attain maximum values. Minor changes occur between 10 and 15 cm, where the scores on the first factor are somewhat lower (as a result of the lower relative frequencies of N. turgida and H. pacljica), and in the uppermost part of the core, between 2 and 4 cm, where the low values on the first axis are again resulting from lower percentages of N. turgida. Factor 2 is positively loaded by E. vitrea and B. marginata, and negatively by Elphidium spp. and Asterigerinata adriatica. The main turnover points on this axis are at the 45 and 20 cm levels. The lowest level coincides with the level where the epiphytic fauna1 elements are gradually disappearing, and are replaced by a number of mud-dwelling taxa. The second turnover point is the level where N. turgida attains maximum values at the expense of E. vitrea and B, marginata. Summarizing, the fauna1 patterns show a number of significant changes over the studied interval. Both at the 50 and the 40 cm levels there is some evidence for an increase in sedimentation rate, albeit without significant changes in grain size. Coincidently, the fauna1 patterns show a change to faunas which are increasingly dominated
D.M.
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Geology 122 (1995)
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367-384
.9 I Ammonia perlucida Elphidium paeyonum Elphidium granasum Reussello spinulaso Elphidium odvenum Text&aria aggiutinans Cibicides labatulus Buccello gronulata Cavelinaosis oraeaeri Elphidiu& spp. ~a Asterioerinato odriatico Amm&ia porkinsoniono Cassidulina crossa Pseudaepanides foisabeccarii Quinquelaculina seminulo Bulimino marginato Sigmailapsis schlumbergeri Epistaminella exiguo Eggerello scobro Balivina dilototo, striatula-type Balivina spathulato Maruloeplecto bulbasa Stainfatihio fusifarmis Balivino dilatata, typica I Balivina seminuda Nanianella turgida Quinqueloculino stolkeri Hapkinsina pocifico
III B
III A
Fig. 5. Dendrograrn
resulting
from a cluster
analysis
on the basis of the relative frequencies
by mud-dwellers, and in which epiphytic taxa become rare. At the 20 cm level, a major turnover point is shown on both PCA axes, apparently completely unrelated to any substantial changes in grain size. Finally, some changes of minor extent seem to be present in the top part of the core.
6. Discussion The peculiarity of finding an association with epiphytic elements in the basal part of the core, witnessing some type of vegetation cover in the PO delta region, suggests that the situation in the first half of the nineteenth century was drastically different from the present-day one. Ciabatti (1966), Nelson (1970), Gandolfi et al. (1982) and Boldrin et al. (1988) all refer to the historical changes which took place during the past centuries. Gandolfi et al. (1982), who document the changes since pre-Etruscan time, show that the outflow pattern of the PO, both in terms of amount and loci of discharge, changed substantially due to human activities. Deforestation and interference
of the 28 most frequent
taxa.
with the natural course of the PO river (canals, dikes) were the main factors. The variation in humidity and discharge, which can be considerable (Dal Cin, 1983), has been a third factor of importance. Ciabatti (1966) documents in quite some detail the changes of the past few centuries. Outstanding from this work are the important geographical shifts of the major outlet canals of the PO river as a result of human activity. In Fig. 7 the situation prior to 1840, between 1840 and 1870, and after 1870 (essentially the present-day situation) are given. It can been seen that before 1840 the main PO outlet was the PO di Maestra. According to Gandolfi et al. (1982) the coastline was located considerably more land-inward than at present. Consequently, the major sediment load was transported through the PO di Maestra and diverted southward by the long-shore current, bypassing the position of core 108. Around 1840 the main course of the PO was diverted southward to the PO della Tolle and the PO di Goro. The likely consequence of this is indicated in Fig. 7b: now the outflowing waters and sediment load are more likely to have reached
D.M. Barmawidjaja et al./Marine Geology 122 (1995) 367-384
380 factor
-2 .!5 L 8
1
factor
2
0
.c 5 % 0
10
t 20
30
40
50
-I
3
2 108 0
Fig. 6. Score plots on the first two (significant) factors of the principal components analysis. /
the locality of core 108. Around 1870 finally, the recent situation, with the PO della Pila as most important outlet, was reached (Fig. 7~). Probably this configuration led to a second increase of sediment supply to station 108. It is to be expected that such substantial changes in the sedimentary regime had widespread consequences. Indeed, the historical record fits rather well with the age estimates of our observed faunistic changes. As remarked earlier, our age model
,
Fig. 7. Simplified maps (after Ciabatti, 1966) of the PO delta area, showing the main outlet channels prior to 1840 (top), between 1840 and 1870 (middle) and from 1870 on (bottom).
only provides reliable constraints for the top part of the core. If we extrapolate our age model to the lower part, it can be dated as older than 1850 AD. The timing of the two main events in total numbers (Figs. 4 and 5), situated at 50 cm (1849 AD) and
D.M. Barmawidjaja et al.lk4arine Geology 122 (1995) 367-384
40 cm ( 1877 AD), respectively, coincides remarkably well with the timing of the shifts of the PO outlet channels. Since the sedimentation rate may indeed have increased significantly during the deposition of the core, we are dealing here with a minimum age estimate. The probable consequences of the increased load of fine-grained sediments are an increased sediment accumulation rate and destruction of the vegetation due to the mud load and/or the increased turbidity of the water column. Ultimately this resulted in complete disappearance of vegetation and the related epiphytic life. Also the second step seems to be controlled by the sedimentary patterns. From about 1840 on we see a relative increase of a number of taxa belonging to clusters IIIb and II. The ecology of most of these benthic foraminifera is discussed in some of the more recent papers (Von Daniels, 1970; Jorissen, 1987, 1988; Van der Zwaan and Jorissen, 1991; Jorissen et al., 1992; Barmawidjaja et al., 1992). In Table 2 the ecological characteristics are summarized and reference is made to the degree of opportunism of species based on their distribution with respect to food enrichment and oxygen concentration. Basically, a high degree of opportunism implies a preference for food-enriched conditions in combination with a high tolerance to stressed conditions, in the northern Adriatic Sea particularly due to oxygen deficiency. At 52 cm (1843 AD) A. perlucidu shows a strong increase, at 47 cm ( 1857 AD) followed by E. vitrea, and at 44 cm (1866 AD) by B. marginata. In the same period most taxa of cluster IIIa show a regular decrease in relative frequency, whereas the supposedly epiphytic taxa subsequently disappear completely. From 40 cm ( 1877 AD) on, a mud-dwelling association dominated the site of core 108. The first taxa with increasing abundances (clusters IIIb and II) are all typical for an initial stage of nutrient enrichment, but are not very tolerant for low oxygen concentrations. This indicates that although the sediment load and probably also the nutrient load increased, the environment was not yet stressed. In this sense, the pattern indicates a pre-pollution increase of nutrient supply in muddy environments close to the river mouth, likely related to the final shift in PO outflow patterns around 1870 AD (Table 3).
381
Table 2 Ecological significance of benthic foraminiferal taxa, interpretations are based on Jorissen, 1987 (1) 1988 (2), and Jorissen et al., 1992 (3) Taxon
Environment (Reference)
Cluster Ia: Hopkinsina pactjica Quinqueloculina stalkeri Nonionella turgida Bolivina seminuda Bolivina dilatata, typical
Stainforthiafistformis Morulaeplecta bulbosa Bolivina spathulata
MO1 (3) MO1 MO1 MO2 MO2 MO3 MO2
(3) (3) (3) (3) (3) (3)
Cluster Ib: B. striatula, striatula-type Eggerella scabra
MO1 (3) MO4 (3)
Cluster II: Epistominella vitrea Sigmoilopsis schlumbergeri Bulimina marginata Quinqueloculina seminula Pseudoeponides falsobeccarii Cassidulina crassa
MO2 (3) M (1,2) MO2 (3) S/M (132) M (1,2) _
Cluster IIIa: Ammonia parkinsoniana Asterigerinata adriatica Elphidium spp. Gavelinopsis praegeri Buccella granulata Cibicides lobatulus Textularia agglutinans Elphidium advenum Reussella spinulosa
M/S (192) _ S/M, E (1) S/M, E? (1,2) S/M, E (1,2) MO4 (3) M (1,2) S/M, E? (1,2)
Cluster IIIb: Elphidium granosum Elphidium poeyamun Ammonia perlucida
M/S (2) MIS (2) M/S (2)
MOl-M04: taxa typical for muddy (enriched, seasonally stressed) substrates, with (from 1 to 4) a decreasing degree of opportunism. M: taxa typical for muddy substrates, which are relatively poor in food, and unstressed. S: taxa typical for sandy substrates. E: taxa with an epiphytic mode of life.
The youngest stages in the fauna1 development are not readily explained by changes in the sedimentary regime. Sedimentary texture (e.g. grain size) and structure (i.e. bioturbation) remained basically unaltered but substantial fauna1 changes occurred. From about 1880 AD the taxa of clusters IIIb and II were very gradually replaced by the
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et al./Marine
Table 3 Summary of eutrophication history inferred from important fauna1 changes and possible sources of change as discussed in the text Event
Source
1830 AD: base of core 1840 AD: increase sediment load
diversion of PO outflow
1870 AD: final disappearance of vegetation due to mud load and natural eutrophication
diversion of PO outflow to present position
1880-1920 AD: gradual increase of eutrophication
man-induced increase of PO nutrient load
1930 AD: acceleration of eutrophication increase
modem farming methods, increase of industrialisation and urbanisation
1960 AD: increase of seasonal anoxia
intensification of eutrophication due the maninduced increase of PO nutrient load
1981-1987 AD: maximum of idem anoxia
more stress-tolerant taxa of cluster I. This is most clear in N. turgidu, which starts to increase at 34 cm (1894 AD). N turgidu is an epifaunal species (Barmawidjaja et al., 1992), tolerant to oxygen stress. In the present day Adriatic Sea it occurs abundantly in the mud zone resulting from the outflow of the PO plume, indicating that it is a highly opportunistic species, which is able to proliferate in nutrient-rich environments, even when oxygen concentrations are periodically very low. Its steadily increasing abundance pattern suggests a continuously increasing nutrient enrichment of the northern Adriatic Sea. A next major turnover seems to take place between 24 and 18 cm, around 1930 AD. The scores on the first principal component reach maximal values and those on the second factor shift to negative values. This is clearly caused by the increasing dominance of a number of opportunistic, stress tolerant taxa (H. paczjica, Bolivina seminuda and Quinqueloculina stalkeri; see Fig. 4, compare Table 2) at the expense of other species. The series of events shows that from 1930 onwards, the oxygen-tolerant taxa of cluster I are more and
Geology 122 (1995) 367-W
more advantaged with respect to less tolerant taxa of cluster II, suggesting that oxygen shortness starts to be an ecological factor of importance. Between 14 and 10 cm (around 1960 AD) a next fauna1 adjustment takes place. The percentages of Eggerella advena, Morulaeplecta bulbosa and Reophax nana, all very fragile arenaceous taxa, increase, and H. paczjica reaches maximum values (see Table 1). This event strongly suggests that at 1960 anoxic events became a common phenomenon. H. pacz@a is probably our most stresstolerant taxon, whereas the increased numbers of the arenaceous taxa can be explained by the increased preservational potential. These taxa tend to decompose quite rapidly under oxic conditions (Bizon and Bizon, 1985). The influence of oxygen on the preservation could also explain the striking minimum of N. turgidu from 3 to 1 cm (1981-1987 AD), which apparently is in contrast with the trend of increasing eutrophication. Together with a number of miliolid taxa, the very fragile N. turgidu is among the taxa most sensitive for dissolution. If, as we suspect, the 198 1-1987 minimum of this taxon is indeed resulting from dissolution, then this would indicate that anoxia were still becoming more intense during the last decennium. An additional argument for the importance of dissolution is the fact that the relative numbers of H. paczjica and Stainforthia fusiformis are much higher in the living associations found at station 108 (Barmawidjaja et al., 1992) than in the present samples. In theory, the fauna1 changes discussed could have been induced by changes in the deltaic system or variation in the discharge volume. This is not supported by the historical records as discussed earlier or by the discharge record of the PO since 1918 (Dal Cin, 1983), which shows clearly that the pattern of the annual discharge volume is not reflected in our faunistic record. Degobbis et al. (1979), however, do suggest that variation in discharge volume is an important factor. Clearly, the human-induced nutrient load carried by the PO into the Adriatic Sea has increased over the years, and seems to be the most likely factor to explain the fauna1 patterns. The natural and anthropogenic dissolved nutrient and particulate load, which the PO river is bringing into the
D. M. Barmawidjaja et al. JMarine Geology 122 ( 1995) 367-384
marine realm, leads to considerable eutrophication of an otherwise rather oligotrophic system (Stirn, 1973; Degobbis et al., 1979; Chiaudani et al., 1983; Giordani and Angolini, 1983; Ivancic and Degobbis, 1987; Justic, 1987). Between 1968 en 1980, the nutrient load carried by the PO river more than doubled (Marchetti et al., 1989). It has been well established now that the nutrient load and the subsequent primary production lead to anoxia during late summer and autumn over increasingly larger areas (Faganeli et al., 1985; Justic, 1987; Justic et al., 1987). Apart from the organic pollution, there is considerable (especially post-war) inorganic pollution (e.g. Guerzoni et al., 1984; Pavoni et al., 1987). Anoxia have been known for centuries in the Adriatic Sea (Justic, 1987), although they seem to be more common since a few decades. Justic ( 1987) and Justic et al. (1987) present evidence that in the period between 1911-1913 and 1955-1966 already considerable changes took place in the Adriatic Sea with respect to especially the surface water oxygen contents. Supersaturation likely occurred just in front of the PO outflow. Later on, between 1955-1966 and 1972-1982, the picture changed dramatically. In that period, the likelihood of the occurrence of supersaturation in surface waters and anoxia in bottom waters became widespread. These studies suggest that eutrophication would already mark the history of the Adriatic Sea for some 75 years. The steadily increasing trend of N. turgidu from about 1900 AD onwards indicates that the nutrient load and consequent stress on the benthic system increased since then. Since we find no correlation with the discharge records of the PO, we think that the conclusion is justified that the human induced nutrient load, especially phosphates, has increasingly been eutrophicating the Adriatic Sea since the beginning of this century, but in particular during the post-war period. This is confirmed by the pattern of H. paciJica and B. seminude, which at present belong to the most tolerant taxa (Jorissen et al., 1992) and which show a strong increase at about 1930 AD. Especially the record of these two species could indicate that anoxic or dysoxic conditions started to appear since that time. This conclusion would be in line with the
383
conclusion drawn by Justic (1987) although our data indicate that the eutrophication started somewhat earlier than was assumed by Justic. Around 1960 anoxia apparently became a regular phenomenon. The synchroneity of the onset of stressed conditions, and the doubling of the nutrient load of the PO between 1968 and 1980 (Marchetti et al., 1989) is remarkable. Finally, if we interpret the fauna1 signal correctly, even the strong increase of anoxia in the last decennium is reflected in our fauna1 curves.
7. Conclusions The benthic associations of core 108 perfectly record the youngest environmental history of this part of the northern Adriatic Sea. However, since only one core could be studied with the extremely high resolution as described here, our data base is limited; consequently, the conclusions have to be regarded as tentative and possibly not applicable to the whole northern Adriatic region. Our data suggest that two significant (man-induced) shifts of the main PO outlets, as documented in historical records, led to substantial changes in the sedimentation and fauna1 patterns in front of the PO delta. Between 1800 and 1840, a first shift led to a substantial increase of the mud and nutrient load arriving at the core locality. The existing vegetation cover was damaged and the relative importance of epiphytic elements in the fauna1 association decreased considerably. After a second shift, around 1870 when the PO della Pila became the most important outlet, the fauna consisted almost exclusively of mud-dwellers, indicative of natural, pre-industrial nutrient levels. Since 1900 there has been a steady trend indicating of nutriflcation, initially mainly indicative by rising percentages of Nonionella turgida. A major step in this process can be recognized around 1930, when a number of very stress-tolerant taxa enter the record, or increase substantially in relative abundance. Apparently already at about 1930 the northern Adriatic Sea became strongly eutrophicated. A last fauna1 change from 1960 onwards indicates that seasonal anoxia started to be prominent.
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Acknowledgements We thank M. Reith for the sedimentological analyses, G. van ‘t Veld and G. Ittman for processing the micropaleontological samples, T. van Hinte for preparing the drawings, W.J. Zachariasse and H. de Stigter for commenting on earlier drafts of the manuscript. The collection of the samples was funded by the Ministry of Science, Technology and Informatics of the Republic of Croatia.
References Barmawidjaja, D., Jorissen, F.J., Puskaric, S. and Van der Zwaan, G.J., 1992. Microhabitat selection by benthic foraminifera in the Northern Adriatic Sea. J. Foraminiferal Res., 22: 297-317. Bizon, G. and Bizon, J.J., 1985. Methode d’etudes et mode de prelevement des sediments d’ECOMED. In: J.J. Bizon and P.F. Burollet (Editors), Ecologic des Microorganismes en Mediterranee Qccidentale ‘ECOMED’. Assoc. Fr. Techn. Pet., Paris, pp. 81-83. Boldrin, A., Bortoluai, G., Frascari, F., Guerzoni, S. and Rabitti, S., 1988. Recent deposits and suspended sediments off the PO della Pila (PO River, main mouth), Italy. Mar. Geol., 79: 159-170. Brambati, A., Ciabatti, M., Fanzutti, G.P., Marabini, F. and Marocco, R., 1983. A new sedimentological textural map of the northern and central Adriatic Sea. Boll. Oceanol. Teor. Applic., 4: 267-271. Chiaudani, G., Pagnotta and R. Vighi, M., 1983. Eutrophication in Emilia-Romagna coastal waters: scientific basis for protection actions. Thalassia Jugoslavia, 19: 67-75. Ciabatti, M., 1966. Richerche sull’evoluzione de1 delta padano. G. Geol., Ser. 2, 34: l-26. Dal Cin, R., 1983. I litorali de1 delta de1 PO e alle foci dell’Adige e de1 Brenta: caratteri tessiturali e dispersione dei sedimenti, cause dell’arretramento e previsioni sull’ evoluzione futura. Boll. Sot. Geol. Ital., 102: 9-56. Dal Cin, R. and Simeoni, U., 1987. Analisi ambientale quantitativa dei litorali marchigiani tra Gabicce e Ancona. Live110de1 rischio naturale e de1 degrado, distribuzione dei sedimenti e loro possibile impiego per ripascimenti artificiali. Boll. Sot. Geol. Ital., 106: 377-423. Davis, J.C., 1988. Statistics and Data Analysis in Geology. Wiley, New York, 2nd ed., 550 pp. Degobbis, D., 1989. Increased eutrophication of the Northern Adriatic Sea. Second Act. Mar. Pollut. Bull., 20: 452-457. Degobbis, D., Smodlaka, N., Pojed, Skrivanic, A. and Precali, R., 1979. Increased eutrophication of the Northern Adriatic Sea. Mar. Pollut. Bull., 10: 298-301. Faganeli, J., Avcin, A., Fanulo, N., Malej, A., Turk, V., Tusnik, P., Vriser, B. and Vukovic, A., 1985. Bottom layer anoxia in the central part of the Gulf of Triest in the late summer of 1983. Mar. Pollut. Bull., 16: 75-78.
Gandolfi, G., Mordenti, A. and Paganelli, L., 1982. Composition and longshore dispersal of sands from the PO and Adige rivers since pre-Etruscan age. J. Sediment. Petrol., 52: 797-805. Giordani, P. and Angiolini, L., 1983. Chemical parameters characterizing the sedimentary environment in a NW Adriatic coastal area (Italy). Estuarine Coastal Shelf Sci., 17: 159-167. Guerzoni, S., Ravaioli, M., Rovatti., G. and Suman, D., 1984. Comparison of Z’“Pb, tace metals (Hg, Pb, Cr) profiles and river discharge in a core off the PO della Pila river mouth (Italy). VIIth Journees Etud. Pollutions. (Lucerne.) CIESM, pp. 303-307. Ivancic, I. and Degobbis, D., 1987. Mechanisms of production and fate of organic phosphorus in the Northern Adriatic Sea. Mar. Biol., 94: 117-125. Jorissen, F.J., 1987. The distribution of benthic foraminifera in the Adriatic Sea. Mar. Micropaleontol., 12: 21-48. Jorissen, F.J., 1988. Benthic foraminifera from the Adriatic Utrecht variation. of phenotypic Sea; principles Micropaleontol. Bull., 37, 176 pp. Jorissen, F.J., Barmawidjaja, D.M., Puskaric, S. and Van der Zwaan, G.J., 1992. Vertical distribution of benthic foraminifera in the northern Adriatic Sea: The relation with the organic flux. Mar. Micropaleontol., 19: 131-146. Justic, D., 1987. Long term eutrophication of the Northern Adriatic Sea. Mar. Pollut. Bull., 18: 281-284. Justic, D., 1988. Trend in the Transparency of the Northern Adriatic Sea 1911-1982. Mar. Pollut. Bull., 19: 32-35. Justic, D., Legovic, T. and Rottini-Sandrini, L., 1987. Trends in oxygen content 1911-1984 and occurrence of benthic mortality in the northern Adriatic Sea. Estuarine Coastal Shelf Sci., 25: 435-445. Marchetti, R., Gaggino, G.F. and Provini, A., 1988. Red tides in the Northwest Adriatic. Unesco Rep. Mar. Sci., 49: 133-142. Marchetti, R., Provini, A. and Crosa, G., 1989. Nutrient load carried by the River PO into the Adriatic Sea, 1968-87. Mar. Pollut. Bull., 20: 168-172. Nelson, B.W., 1970. Hydropgraphy, sediment dispersal and recent historical development of the PO River Delta, Italy. SEPM Spec. Publ., 15: 152-184. Pavoni, B., Donazzolo, Marcomini, A., Degobbis, D. and Orio, A., 1987. Historical development of the Venice lagoon contamination as recorded in radiodated sediment cores. Mar. Pollut. Bull., 18: 18-24. Puskaric, S., Berger, G.W. and Jorissen, F.J., 1990. Successive appearance of subfossil phytoplankton species of the northem Adriatic Sea and its relation to the increased eutrophication pressure. Estuarine Coastal Shelf Res., 31: 177-187. Stim, J., 1973. Organic pollution as the main factor causing biological disequilibria in coastal waters. Archo Oceanogr. Limnol., 18: 111-119. Van der Zwaan, G.J. and Jorissen, F.J., 1991. Biofacial patterns in river-induced shelf anoxia. In: R. Tyson and T.H. Pearson (Editors), Modem and Ancient Shelf Anoxia. Geol. Sot. London Spec. Publ., 58: 65-82. Von Daniels, C.H., 1970. Quantitative (ikologische Analyse der zeitlichen und raumlichen Verteilung rezenter Foraminiferen im Liiski-kanal bei Rovinj (nordliche Adria). Gijttinger Arb. Geol. Paliiontol., 8: l-190.