1. Effects of aquaculture on Mediterranean marine ecosystems
I. Karakassis, D. Angel

2. Effects of aquaculture on marine biotic communities
(modified after Milowski 2001)

3. Posidonia protects the seabed from errosion
4/14/2017
Posidonia protects the seabed from errosion

4. 4/14/2017
Posidonia rhizomes
Plagiotropic rhizome
Orthotropic rhizome

5. 4/14/2017
Posidonia: provides shelter to juvenile fish and many manire invertebrates
Spp reproducing in P. oceanica meadows
Lithignathus mormyrus
Sparus auratus
Oblada melanura
Sapra sapra
Paracentrotus lividus
Symphodus roissali
Antedon mediterraneus
Murena helena
Conger conger
Lichia amia
Seriola dumerili
Mullus surmuletus

6. Under anthropogenic pressure Posidonia meadows easily become degraded
4/14/2017
Under anthropogenic pressure Posidonia meadows easily become degraded

7. 4/14/2017
… so that its past presence can only be detected by rhizomes left on the seabed

8. 4/14/2017
High turbidity in the water column is known to adversely affect Posidonia
The reduced availability of light reduces the potential space for colonization by Posidonia to a more and more narrow coastal zone

9. During recent years it has been reported that Posidonia oceanica faces strong copetition by Caulepa taxifolia
4/14/2017
C. taxifolia is an alien species that recently invaded W. Mediterranean. It has no local grazers or other means to control its population and it excludes P. oceanica from coastal waters when established there

10. Why Posidonia is of vital importance
Mediterranean endemic (in need of protection under the Habitat Directive)
a nursery ground for several species
provides important services for coastal marine ecosystems (3D habitat for several invertebrate species)
it stabilises the sandy beaches in the littoral zone
under increasing pressure due to anthropogenic effects (pollution, trawling, harbour constructions etc)
under increasing pressure due to nutrient enrichment of the coastal zones and flourish of fast growing macroalgae, e.g. Cladophora spp., Caulerpa sp.

11. Posidonia meadows as fish farming sites
The habitat of P. oceanica (coarse sediment and strong currents) is “ideal” for fish farming since:
it allows rapid dispersion of solute wastes
minimal accumulation of particulates and
excellent oxygenation of the water

12. Posidonia is stressed at farming sites

13. However f/f causes adverse effects on Posidonia by:
reducing penetration or availability of light
immediately under the cages (shadow effect)
due to increased phytoplankton biomass
due to increased suspended particulates
by favouring the growth of epiphytes on Posidonia leaves
competition with fast growing macroalgae
accumulation of OM in the sediments
increasing NH4 and H2S in the sediments

14. Posidonia: primary production near and far from fish farms
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Posidonia: primary production near and far from fish farms
Reference station
Changes in pp by an order of magnitude
Farm sites
Cancemi et al. (2003) Estuar coastal shelf Sci vol56

15. MedVeg sampling sites

16. MedVeg: sampling design
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MedVeg: sampling design
MedVeg Report 2005, unpublished data

17. MedVeg fluxes measured with sediment traps
Alicante
Flux P=0.26*x-0.41
Sounion
Flux P=0.10*x-0.59
MedVeg Report 2005, unpublished data

18. MedVeg Bioassays

19. MedVeg Bioassays * * * * * * * * * * * * * *
Control site
* signif different from control site
MedVeg Report 2005, unpublished data

20. MedVeg Bioassays - Ulva* * * * * * * * * *
Control site
* signif different from control site
MedVeg Report 2005, unpublished data

21. MedVeg: Posidonia mortalities with distance
MedVeg Report 2005, unpublished data

22. MedVeg: Posidonia mortalities with sedimentation rate
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MedVeg: Posidonia mortalities with sedimentation rate
Mortality increases rapidly beyond the sedimentation rate of 6g m-2 d-1
MedVeg Report 2005, unpublished data

23. MedVeg: Posidonia density & cover
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MedVeg: Posidonia density & cover
Decrease close to the farms
MedVeg Report 2005, unpublished data

24. MedVeg: Posidonia biomass
4/14/2017
MedVeg: Posidonia biomass
Decrease close to the farms
MedVeg Report 2005, unpublished data

25. MedVeg recomendations-2
If monitoring studies indicate a decrease in seagrass meadow extension or shoot density, the amount of waste material (as C, N and P loads) must decrease for a equivalent percentage until recovery of the previous conditions. Alternatively, cages should be moved to other sites, according to guidelines reported above.
Concessionaires must present a plan for the monitoring of possible pressures and damages to seagrass beds and include this in the Environmental Agenda for certification ISO14000 and EMAS (Eco-Management and Audit Scheme).
A suitable monitoring program must use reliable techniques and include quality control procedures, and should be based on the rapid assessment techniques as described below

26. MedVeg descriptors/indicators: at individual plant level
Morphometric descriptors
shoot biomass, expressed as the average dry weight of at least ten replicates shoots
Physiological descriptors
total phosphorus content in different tissues, specifically young leaves and rhizomes, expressed as % of dry weight.
total non-structural carbohydrates reserves in rhizomes, expressed as % of dry weight
elemental sulphur content (as μmol per g dry weight) in roots.

27. MedVeg descriptors/indicators:
At population level
shoot density, based in counting the number of shoots inside patches of Posidonia oceanica and expressed as the number of shoots per square meter .
At community level
epiphyte biomass, expressed as the dry weigh of epiphytes in relation of the size of the shoots.
sea-urchin density, based on counting the number of individuals inside patches of Posidonia oceanica and expressed as the number of individuals m-2

28. However...
Our results do not mean that any fish farming activity should be banned at distance less than 800m from any Posidonia oceanica plant in the Mediterranean.
However, adopting this distance could be an appropriate precautionary measure in the vicinity of important and well-developed Posidonia meadows that environmental authorities have set as priority areas for conservation.
Whenever a fish farm is located in the vicinity of seagrass meadows, the health of the seagrass meadow should be annually monitored.
Working definitions of the term "Posidonia meadow" should be harmonised among Mediterranean countries and common standards are set regarding priorities for conservation of such meadows.
Otherwise, it is likely that MedVeg recommendations will be enforced differently in different member states and other Mediterranean countries thereby resulting in both inadequate environmental protection and in violating equal terms of competition within aquaculture industry.

29. Mass balance models
4/14/2017
Detailed mass balance models have been established for salmonid farming
According to these there are some remarcable differences in the amount of soluble and sedimenting proportions between nitrogen and phosphorus
Since no such models exist for the Mediterranean we have used the estimates provided through these models in order to obtain a rough estimate for the additional nutrient loads in the Mediterranean.
Karakassis et al. (2005) Sci Mar vol 69

30. Land-based tanks Diel high frequency sampling experiments on fluxes of
4/14/2017
Diel high frequency sampling experiments on fluxes of
Nutrients
POC
PON
Bacteria
tanks containing
different fish sizes
(1, 31 & 53gr)
input
output
sea bass
Tsapakis, Pitta, Karakassis (2006) Aquat. Liv. Resour vol 19

31. Nutrient dynamics Fish size: 1gr Significant difference and
4/14/2017
Fish size: 1gr
Significant difference and
Diel pattern in discharge
Tsapakis, Pitta, Karakassis (2006) Aquat. Liv. Resour vol 19

32. POC and PON dynamics Significant difference and
4/14/2017
Significant difference and
Diel pattern in discharge
Tsapakis, Pitta, Karakassis (2006) Aquat. Liv. Resour vol 19

33. N & P mass balance: % losses over feed input
4/14/2017 14 13 16
PO4
(%) 26 6
Average 27 7 53 29 5 31 21 1
NH4
PON
Fish Size
(gr)
Fine particulate material settling at very slow rates and over larger distance from the discharge points
Tsapakis, Pitta, Karakassis (2006) Aquat. Liv. Resour vol 19

34. However
4/14/2017
Several studies have failed to detect significant changes in dissolved nutrients, Chl-a and POC concentrations even at fairly short distance from the cages (Pitta et al 1998, La Rosa et al., 2002, MEDVEG unpublished data, Soto & Norambuena 2004)
This paradox might be due to:
The dispersive nature of the sites (nutrients are rapidly diluted)
Inefficient sampling (concentrations vs fluxes)
Intensive grazing and transfer to higher trophic levels
Combination of the above

35. Grazing experiment in Crete using dialysis chambers
4/14/2017
Grazing experiment in Crete using dialysis chambers
filtered 8
Chlorella 6
unfiltered
Chl a (mg l-1) 4 2 30 80
200
>500
Distance (m)
Karakassis et al. (submitted)

36. Local Fisheries landings :time series analysis
Analyses
Local Fisheries landings :time series analysis
Environmental: OC, Chla, Nutrients
Fish: Species, Abundance + Biomass per species, diversity, biodiversity, LF, age, condition factor, fecundity, G Index, stomachs, lipids, proteins
Mega: S, A + B per species, diversity, biodiversity
Macro: S, A, B total, diversity
Bacteria: Counts
Micro zoo + Phytoplankton: S, A, B (total), diversity
Fish spatial structure: geostatistics

37. Fish communities
The communities differed firstly according the substrate and secondly according to fish-farms presence.
The effect of fish-farm presence was mainly quantitative
No significant differences in diversity or biodiversity indices (taxon. distinctness etc)

38. Fish communities
The total abundance and biomass was higher near to fish farms in May – and fairly similar in the recruitment period in September.
It seems that during the recruitment period all sites (Near and Far) are stocked with fish close to the carrying capacity

39. Effects on Landings
Total Landings
Farm Production

40. Effects on Landings: MAFA analysis
The correlation between the size of the fishing fleet & the landings trend could be coincidental: due to a clear declining trend because of a vessel withdrawal policy
Rainfall & Temperature did not show any correlation with the common trend (except Chios)
fish-farming production related to an increase of local fisheries landings A B

41. AQCESS conclusions No change in macrofauna
Small changes in megafaunal biomass
Big change in fish abundance and biomass documented through:
Before-after study: Machias et al 2004, ECSS, v. 60
Near-far study: Machias et al 2005, MEPS, v. 288
Landings: Machias et al. (2006) Aquaculture v. 261
Hydroacoustics: Giannoulaki et al. 2005, JMBA UK v. 85
FAD effect? No, the list of species (<30 spp) aggregating near the cages are known (Dempster et al 2002 MEPS for W. Med, Smith et al submitted from the E. Med). Not the ones increasing in the above studies

42. AQCESS conclusions
Not all benthic communities respond in the same way to disturbance
Large long living animals could be more efficient means for monitoring subtle changes
The most possible explanation is the rapid transfer of nutrients up the food web in a nutrient-starving environment

43. sediment: horizontal changes
4/14/2017
sediment: horizontal changes
current
TOC (%)
TON (%)
Eh (mV)
Cephalonia
Ithaki
Sounion
Karakassis et al. (2000) ICES J mar sci 57

44. Meta-analysis of benthic effects
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Meta-analysis of benthic effects
Kalantzi & Karakassis (2006) Mar. Pollut. Bull vol 52

45. Meta-analysis of benthic effects
4/14/2017
Meta-analysis of benthic effects
Kalantzi & Karakassis (2006) Mar. Pollut. Bull vol. 52

46. Meta-analysis of benthic effects
4/14/2017
Meta-analysis of benthic effects

47. Sediment profiling imagery (SPI): an «inverted periscope»
4/14/2017
Sediment profiling imagery (SPI): an «inverted periscope»
camera
glass
mirror

48. SPI images beneath fish farms
4/14/2017
SPI images beneath fish farms UF
CH4 or H2S FS Bg FS
BLT
BLT BT
Source: Karakassis, Tsapakis, Smith, Rumohr. (2002) Mar Ecol Prog Ser, 227

49. Multivariate analysis of SPI data
4/14/2017
Multivariate analysis of SPI data
October
February
July
Euclidean distance
fauna
SPI
Comparisons between multivariate patterns
Source: Karakassis, Tsapakis, Smith, Rumohr. (2002) Mar Ecol Prog Ser 227

50. Minimizing monitoring requirements
All correlation coefficient values were significant (p<0.001)
Lampadariou, Karakassis, Pearson (2005) Mar. Pollut Bull vol 50

51. Modelling spatial patterns of settling particles
DEPOMOD -> MERAMOD
4/14/2017
A tool for prediction of benthic degradation
High correlation between predicted and observed sedimentation
High correlation between predicted sedimentation and macrofaunal diversity
Cromey et al. in preparation

52. Sedimentation by fish farms
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Sedimentation by fish farms
Detailed mass balance models have been established for salmonid farming
According to these there are some remarcable differences in the amount of soluble and sedimenting proportions between nitrogen and phosphorus
Since no such models exist for the Mediterranean we have used the estimates provided through these models in order to obtain a rough estimate for the additional nutrient loads in the Mediterranean.
* for trout cage farming in Sweden
by Holby & Hall (1991) and by Hall et al. (1992) MEPS

53. effects on benthos Pearson & Rosenberg (1978)
4/14/2017
effects on benthos
The succession pattern described by Pearson & Rosenberg is one of the most robust models in marine ecology
All the work done on benthic communities reveals this general pattern, although different organisms might be involved in different parts of the succession in different parts of the world
Pearson & Rosenberg (1978)

54. Hierarchical response to stress
4/14/2017
Hierarchical response to stress
Pearson & Rosenberg (1978)
Replacement by different order,class, phylum
Replacement by different family
Replacement by different genus
stress
Replacement by different species
Eνα αρκετά γνωστό πρότυπο που σχετίζεται με την απόκριση των βενθικών βιοκοινοτήτων στη διατάραξη είναι η
Replacement by more addapted individuals from a polymorphic stock
Physiological reponse of the individual
time

55. Biotic coefficient (BC) - AMBI
4/14/2017
Biotic coefficient (BC) - AMBI
The BC proposed by Borja et al (2000) distributes species into various groups depending on their ability to tolearate disturbence/pllution
Group I. Sensitive species, present only in complete absence of pollution
Group II. Indifferent species always present in small densities without significant fluctuation with time
Group III. Tolerant species. they may be found under natural conditions but their population growth is stimulated under organic enrichment
Group IV. Second stage opportunists. Mainly small-size subsurface deposit feeders (e.g. Cirratulidae)
Group V. First stage opportunists. Deposit feeders thriving in reduced sediments.

56. Biotic coefficient (BC)
4/14/2017
Biotic coefficient (BC)
The value of BC is then calculated for every sample based on the % of each group on total macrofaunal abundance.
(0xGI)+(1.5xGII)+(3xGIII)+(4.5xGIV)+(6xGV)
BC=
100
This index is supported by a software in EXCEL (AMBI) and a data base providing characterization of >3000 benthic species (
Borja A, Franco J, Perez V (2000) A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Marine Pollution Bulletin 40:1100–1114.
Muxika I, Borja A, Bonne W (2005) The suitability of the marine biotic index (AMBI) to new impact sources along European coasts. Ecol. Indic, 5:19–31.

57. Limits for BC classification BC Dominant group
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Limits for BC
classification BC
Dominant group
Benthic community health
In terms of pollution
Non polluted
0.0<BC
<
0.2 I
normal
Non polluted
0.2<BC
<
1.2
poor
Slightly polluted
1.2<BC
<
3.3
III
unbalanced
Moderately polluted
3.3<BC
<
4.3
Transitional to polluted
Moderately polluted
4.3<BC
<
5.0
IV-V
polluted
Heavily polluted
5.0<BC
<
5.5
Transitional to havily polluted
In oder to assess the level of impact we have sampled the water column in 3 farms x 3 seasons x 3 depths with 5 real replicates
and with a control site in each fram. The idea was to investigate the variability induced by “natural sources” and compare it to the variability induced by f-farming.
Among the nutrients only ammonium ions showed a significant increase exceeding all other sources of variability
However this increase was not transleted into high CHLa nor increased POC or PON which are the variables most relevant to the increase in phytoplankton biomass.
Heavily polluted
5.5<BC
<
6.0 V
Heavily polluted
extremely polluted
αζωική
αζωική
azoic
Borja et al (2000) Mar Pollut Bull –1114.

58. 4/14/2017
BENTIX
BENTIX (Benthic index) is a variation of BC proposed by greek scientists (Simboura &, Zenetos 2002)
The difference from BC is that BENTIX recognizes only 3 groups of species and the list of species for which there is some characterization is not available except the first edition in Mediterranean Marine Science.
Because BENTIX is calculated giving high scores to intolerant species low values indicate degradation whereas high values «pristinity»
Simboura N, Zenetos A. (2002) Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems including a new Biotic index. Mediterranean Marine Science 3:77–111.

59. 4/14/2017
BC and BENTIX
Both methods are based on subjective judjment on the ecological role of benthic species
Their use needs communication with the authors (direct or indirect through their web page) and up to a point confidence in their oppinion.
The role of each species and the assignment of one group is inflexible and is given only once.
There is no agreed procedure for revising the classification of a species in the groups of each index
The thershod values assigned are more or less arbitrary.

60. Benthic quality index (BQI)
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Benthic quality index (BQI)
BQI (proposed by Rosenberg et al 2004) is somehow different than the previous indices.
Species are not divided into categories but they receive a score depending on their disdtribution in a set of samples
The index is based on the assumption that opportunistic species are primarily found in stations/samples with low diversity whereas the «normal» or sensitive species in stations/samples with increased diversity.
Therefore if the distribution of a species is determined over a series of samples covering a wide range of diversity then the distribution pattern will vary from species to species depending on their sensitivity or tolerance.
Rosenberg R, Blomqvist M, Nilsson HC, Cederwall H, Dimming A (2004) Marine Pollution Bulletin 30 (7), 470 –474

61. Calculation of ES500.05 disturbed undisturbed
4/14/2017
Calculation of ES500.05
The shaded area includes the 5% of the total abundance of the species which is related to low diversity stations
In oder to assess the level of impact we have sampled the water column in 3 farms x 3 seasons x 3 depths with 5 real replicates
and with a control site in each fram. The idea was to investigate the variability induced by “natural sources” and compare it to the variability induced by f-farming.
Among the nutrients only ammonium ions showed a significant increase exceeding all other sources of variability
However this increase was not transleted into high CHLa nor increased POC or PON which are the variables most relevant to the increase in phytoplankton biomass.
disturbed undisturbed
Rosenberg R, et al. (2004). Mar Pollut. Bull. 30:470 –474

62. Calculation of ES500.05 for various species
4/14/2017
Calculation of ES for various species
In oder to assess the level of impact we have sampled the water column in 3 farms x 3 seasons x 3 depths with 5 real replicates
and with a control site in each fram. The idea was to investigate the variability induced by “natural sources” and compare it to the variability induced by f-farming.
Among the nutrients only ammonium ions showed a significant increase exceeding all other sources of variability
However this increase was not transleted into high CHLa nor increased POC or PON which are the variables most relevant to the increase in phytoplankton biomass.
Low values: tolerant species, High values: sensitive species
Χαμηλές τιμές: ανθεκτικά είδη, Υψηλές τιμές: ευαίσθητα είδη
Rosenberg R, et al. (2004). Mar Pollut. Bull. 30:470 –474

63. Benthic quality index (BQI)
4/14/2017
Benthic quality index (BQI)
After calculating ES for each species, BQI is calculated for each sample:
BQI= x ES x 10log(S+1) ( ) n Σ
i=1 ( Ai )
tot A

64. BQI and sediment condition
4/14/2017
BQI and sediment condition
SPI images
Condition in relation to Pearson & Rosenberg 1978
In oder to assess the level of impact we have sampled the water column in 3 farms x 3 seasons x 3 depths with 5 real replicates
and with a control site in each fram. The idea was to investigate the variability induced by “natural sources” and compare it to the variability induced by f-farming.
Among the nutrients only ammonium ions showed a significant increase exceeding all other sources of variability
However this increase was not transleted into high CHLa nor increased POC or PON which are the variables most relevant to the increase in phytoplankton biomass.
Thresholds and sediment quality
Rosenberg R, et al. (2004). Mar Pollut. Bull. 30:470 –474

65. 4/14/2017
Hypotheses to test
Do all these indices describe the conditions similarly?
Are they intercorrelated?
Do they depend on sieve size?
Do they depend on season?
Do they assign the same environmental quality to the samples examined?

66. Sieve size Highly correlated y=1.0*x Good news ! Values at 1.0 mm
4/14/2017
Sieve size
Highly correlated
y=1.0*x
Good news !
Values at 1.0 mm
Values at 0.5 mm

67. season Highly inter- correlated for most indices
4/14/2017
season
Highly inter- correlated for most indices
Relatively Good news !
Spearman rank correlation
index

68. Do they intercorrelate?
4/14/2017
Do they intercorrelate?
Highly inter- correlated (p<0.01) for most indices
Relatively Good news !
So we can chose any of them without worrying?

69. 4/14/2017
How similar they are?
Using the correlation matrix we can run an MDS and obtain similarities among indices D+ L+
AMBI
BENTIX H’
BQI
Stress:0.01

70. Do they agree in Environmental status?
4/14/2017
Do they agree in Environmental status?
Well… No
In fact they reach a «consensus» in 4% of the samples and they had 3-4 different «verdicts» in 39% of the samples
bad
poor
moderate
good
high

71. Are there consistently easy-to-pass and difficult ones?
4/14/2017
Are there consistently easy-to-pass and difficult ones?
Yes BENTIX and H’ tend to show more High and Good quality
BQI tends to show (reveal?) more Bad and Poor conditions

72. 4/14/2017
furthermore
The Pearson & Rosenberg model works well with silty sediments
For coarse sediments it is possible to have a “healthy picture” despite the fact that environmental degradation may have severely affected other components of the ecosystem.

73. 4/14/2017
Χαρακτηριστικά των ιχθυοτροφείων στο δείγμα (fish farms characteristics)
% ιλύος αργίλου
(% silt-clay)
Βάθος (m) depth
Παραγωγή (τόνοι/έτος)
Production (tn/year)

74. Αριθμός ειδών (species number)
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Αριθμός ειδών (species number)
Minimum=5spp
# species
Minimum=32spp
Παραγωγή (τόνοι/έτος)
Production (tn/year)

75. Μέσος αριθμός ειδών (average species number)
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Μέσος αριθμός ειδών (average species number)
Average # species
Απόσταση Distance

76. Δείκτης Shannon (Shannon index)
4/14/2017
Δείκτης Shannon (Shannon index)
H’ (bits)
Παραγωγή (τόνοι/έτος)
Production (tn/year)

77. Δείκτης Shannon (Shannon index)
4/14/2017
Δείκτης Shannon (Shannon index)
H’ (bits)
Απόσταση Distance

78. Δείκτης Bentix (BENTIX index)
4/14/2017
Δείκτης Bentix (BENTIX index)
Poor-bad
Bentix index
Poor-bad
Παραγωγή (τόνοι/έτος)
Production (tn/year)

79. Δείκτης AMBI (AMBI index)
4/14/2017
Δείκτης AMBI (AMBI index)
Poor-bad
Poor-bad
AMBI index
Παραγωγή (τόνοι/έτος)
Production (tn/year)

80. Δείκτης AMBI σε όλα τα δείγματα (AMBI index, all samples & stations)
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Δείκτης AMBI σε όλα τα δείγματα (AMBI index, all samples & stations)
AMBI categories (%)
Απόσταση (m) Distance

81. Δείκτης Shannon σε όλα τα δείγματα (H’ index, all samples & stations)
4/14/2017
Δείκτης Shannon σε όλα τα δείγματα (H’ index, all samples & stations)
Shannon categories (%)
Απόσταση (m) Distance

82. 4/14/2017
Δείκτης BENTIX σε όλα τα δείγματα (BENTIX index, all samples & stations)
BENTIX categories (%)
Απόσταση (m) Distance

83. 4/14/2017
Thank you