Comparison between trophic models of protected and fishing areas

ICES CM 2005/BB:11
Comparison between trophic models of protected and fishing areas for an
ecosystem approach to fisheries in Adriatic Sea
Simone Libralato 1,*, Marta Coll 2, Alberto Santojanni 3, Cosimo Solidoro 1, Enrico Arneri 3 and Isabel
Palomera 2
1
Istituto Nazionale di Oceanografia e di Geofisica Sperimentale – OGS, Borgo Grotta Gigante 42/c, 34010, Sgonico (TS),
Italy
2
Institut de Ciènces del Mar, CMIMA-CSIC, Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain
3
Istituto di Scienze Marine (CNR), Sezione Pesca Marittima, Largo Fiera della pesca, 2 - 60125 Ancona, Italia Italy
Abstract
The Adriatic Sea is one of the most productive areas in the Mediterranean basin. Because of this, an
ecosystem based approach to fisheries management seems particularly appropriate, since it allows to
account for the effects of both fishing and environmental pressures, along with their indirect and
cascading effects on the trophic web. Mass-balance models, although static pictures of the ecosystem,
can be a valuable tool in giving information on structure and functioning of the ecosystem, in
evidencing effects of fishing and in allowing inference on management options at ecosystem scale.
Comparison between models of exploited and non-exploited sub-systems can offer valuable insight,
too. Here we compare two ecological models describing a protected and a non protected area for the
same ecosystem, i.e., the Adriatic Sea. The former represents the MPA of Miramare (Gulf of Trieste,
Italy). The latter represents the fished North and Central Adriatic Sea. The study is the first example of
this kind of comparison in the Mediterranean Sea. In order to have meaningful result, model first were
standardized and then compared on the basis of biomass and flows of production and consumptions
aggregated into integer trophic levels and analyzed in terms of their trophic spectra. The comparison
evidences similarities between the two food webs and differences due to intrinsic features of both areas.
However, differences in the functional role of analogous trophic groups and in ecosystem structure are
also highlighted, thus indicating functional changes that fisheries might have induced. Analyses applied
to the exploited ecosystem model highlights the effects of fishing on target and non target species, and
results are discussed in relation with the observations on the MPA model.
Keywords: ecosystem approach to fisheries; fisheries impact; fisheries management; ecological
models; marine protected area; Adriatic Sea.
* Contact author: Simone Libralato: Dept. Oceanography, Istituto Nazionale di Oceanografia e di
Geofisica Sperimentale – OGS, Borgo Grotta Gigante 42/. 34010 Sgonico (TS), Italy [tel: +39 040
2140376, fax: +39 040 2140266, e-mail: [email protected] ]
1
Introduction
Exploitation of marine resources produces impacts at all ecological levels, i.e. population, community,
habitat and ecosystem, and thus, an ecosystem approach for the management of fisheries is nowadays
recommended (ICES 2001). One of the tools used for an ecosystem approach to fisheries is the
modeling approach of marine trophic webs (Hollowed et al., 2000; Yodzis, 2001; De Young et al.,
2004; Hall and Mainprize, 2004; Pikitch et al., 2004; Maury and Lehodey, 2005), but, for an attempt in
providing useful scenarios for fisheries management, complex ecosystem models need to be calibrated
against time series and the lack of data allow their direct application only in few cases (Walters et al.,
2005).
Nevertheless, the comparison of static trophic web models describing areas subjected to different
exploitation pressures, and particularly the comparison between exploited and protected areas, can
provide useful insights on differences in ecosystem functioning attributable to fishing effects (JarreTeichmann, 1998; Libralato et al., 2002; Moloney et al., 2005). MPAs represent a quasi-natural system
thus useful as comparative systems against exploited ones (Sala et al., 2002), although surrounding
fisheries can have important indirect effects on the trophic structure and functioning of MPAs food web
(Walters, 2000; Salomon et al., 2002). At the moment, MPAs are considered, beside valuable tools for
the maintenance of biodiversity and the conservation of habitats, as the most effective practice for the
management of natural resources otherwise depleted by fisheries (Roberts et al., 2002; Gewin, 2004).
The aim of this work is to compare mass-balance ecosystem models of exploited and protected areas in
the Adriatic Sea in order to identify differences in ecosystem functioning attributable to fisheries
operating in this area. We used two mass balance models, one representing the Central and North
Adriatic fished ecosystem (Coll et al., submitted) and the other describing one of the oldest marine
reserve in Italy, the Riserva Naturale Marina di Miramare, located in the North Adriatic (Tempesta,
2005). This analysis represents a quite novel attempt, since ecological models of protected and non
protected areas for the same system are available for the first time in the Mediterranean Sea. Both food
web models were built by using Ecopath with Ecosim software package version 5.1
(www.ecopath.org), which implements several routines for the application of analysis and aggregation
of flows, estimation of ecological indices and network analysis (Christensen and Walters, 2004).
However, since some outputs and analyses of food web models are influenced by the number of
compartments and aggregation used for representing food webs (Abarca-Arenas and Ulanowicz, 2002;
Dunne et al., 2002; Angelini and Agostinho, 2005), a standardization of both models was necessary
before developing the comparison of models’ results. This prompted two new models for the area, each
made by 16 functional groups. It is expected that groups that occupy similar ‘niche’ in the two model
structures provide similar ecological functions, even if they represent different ensemble of species.
Conversely, a given species might be represented in different functional groups in the two models due
to its different ecological role in the two contexts. We believe that analysis of those differences will
provide additional insight in ecosystem functioning.
2
Materials and Methods
Food webs of protected and fished ecosystem
The food web model of the Miramare Natural Marine Reserve (Riserva Naturale Marina di Miramare)
represents a small protected area in the Gulf of Trieste, where fishing is not allowed since 1986 (D.M.,
1986). The original model for this area, which describes the protected ecosystem in the year 2003
through 19 functional groups (Tempesta, 2005; Libralato et al., submitted), was improved on the basis
of new data available and updated in order to include jellyfish, cephalopods, seabirds and large
predators. The updated model for Miramare Reserve (RNMM food web) accounted for 23 functional
groups and describes the food web of the years 2000-2003.
The food web model for the fished North and Central Adriatic ecosystem for the 1990s (NCA food
web) was previously developed for the analysis of fisheries impact on ecosystem (Coll et al.,
submitted). The model represents the North and Central Adriatic food web, one of the most exploited
ecosystem in Mediterranean, and excludes the eastern part (Slovenia and Croatia’s EEZ) and 3 NM
from the coast. It is composed of 40 functional groups (compartments) each representing one or more
ecologically similar species and is also incorporating the main fishing fleets operating in the area, i.e.
bottom trawling, beam trawling, mid-water trawl, purse seine and tuna fishery and their by-catch and
discards.
The two models were standardized accordingly to a standard structure defined on the basis of broad
ecological groups occupying functional niches that can be identified in all Mediterranean marine
ecosystems. Therefore the standard structure accounts for 16 functional groups (Table 1) and it is
believed to be generally applicable for Mediterranean marine ecosystems. Then, functional groups of
the two original models were aggregated in the identified groups of the standard model, as reported in
Table 1, thus obtaining standardized food web models for exploited North and Central Adriatic Sea and
for Miramare Reserve useful for the comparison. Despite the small number of groups of the
standardized models, they provide examples of a reasonable and general representation useful for
Mediterranean ecosystems.
Analyses of food web outputs
Food web models allowed estimating trophic level (TL) and ecotrophic efficiency (EE) of each
functional group represented. TL is defined as the average number of food interactions (steps) that
allow energy to be transferred from primary producers and detritus to the given functional group
(Lindeman, 1942) and it is estimated as the average trophic level of prey weighted by their proportion
in the diet of the predator (Pauly et al., 1998). The average trophic level of the community (TLco),
excluding TL = 1, reflects the structure of the community and is estimated as the weighted average of
the TL of all the species within the ecosystem (Rochet and Trenkel, 2003). EE is the fraction of
production of the functional group used within the food web by predators and fisheries, thus 1-EE
represent the unexplained natural mortality (Christensen et al., 2000).
The flows of a food web aggregated into integer trophic levels allow constructing simplified
representations of the ecosystem such as the Lindeman Spine, which can provide useful insights on
main flows pathways (Ulanowicz, 1986; Wulff et al., 1989). Moreover, aggregation of flows allows
estimating the transfer efficiency (TE) for energy flowing from one integer trophic level to another: the
TE for a given TL is thus expressed as the ratio between production of TL and production of TL-1
3
(Christensen et al., 2000). In the present work, the Lindeman Spine was modified for representing food
web flows into the two classical food chains: detritus-based and grazing food chains.
Several indices can be used for a comprehensive description of the food web, such as ecological indices
(Odum, 1969), informational theory indicators (Ulanowicz, 1986) and network analysis measures
(Finn, 1976). These indices are commonly used to evaluate degree of development, maturity and
stability of ecosystems (Christensen, 1995; Dunne et al., 2002) and can be computed easily by using
Ecopath (Christensen et al., 2000).
In addition, it is possible to estimate direct and indirect effects that each functional group has on all the
other groups of the web by using input-output analysis (Ulanowicz and Puccia, 1990). Eventually, the
sum of absolute values of mixed trophic impacts for each functional group will allow to infer the total
impact that one species has on all the food web (Libralato et al., 2005), and enables one to assess
relative importance of functional groups and to identify key groups (Power et al., 1996; Piraino et al.,
2002).
Finally, the trophic spectra analysis will be used to enlight differences in productivity and standing
stocks over trophic levels, thus providing insights on ecosystem functioning and effects of fishing
(Guascuel et al., 2005). Since TL for each functional group is estimated with a standard deviation
quantified in the index of omnivory (Christensen et al., 2000), we assumed variables (biomass,
production or catch) for each functional group as being normally distributed with mean=TL and
standard deviation = omnivory index. In this way discontinuity of variables along TL – which can
influence results – are avoided. Since no real TL can exist between TL=1 and TL=2, the trophic
spectrum is obtained by the sum of all the normally distributed values for all TL greater than 2 and the
part of distribution that fall below TL=2 are mirrored and added to values of TL>2. This procedure
represents an improvement on the presently used methodology for the analysis of spectrum of
production, biomasses and catches over trophic levels.
Results
Trophic webs of Adriatic Sea (NCA) and Miramare Reserve (RNMM) showed large differences in
abundances and production of the functional groups (Fig. 1A and B respectively). Seabirds (functional
group number 15) and primary producers (1) are two orders of magnitude more abundant in RNMM
than in NCA food web, while density of top predators (13) is two fold lower in Miramare than in
Adriatic Sea (Fig. 1A). In terms of production (Fig. 1B) suprabenthos (4), top predators (13) and
benthic invertebrates (6) showed values two orders of magnitude higher in NCA than in RNMM.
Seabirds (15) and non piscivorous fishes (11) show higher production in Miramare than Adriatic food
web. However, total biomass and production for all fish groups, all invertebrates and all consumers in
the two trophic webs showed similar values (red dots in Fig. 1A and 1B).
For most of the functional groups very similar trophic levels were estimated in the two food webs (Fig.
2A), with appreciable differences only for jellyfish (3), decapods (7) and non piscivorous fishes (11),
all with higher TL in the NCA food web. Ecotrophic efficiency (Fig. 2B) estimated for each functional
group was similar in the two food webs only for few cases, i.e., for seabirds (15), decapods (7) and
benthopelagic fishes (10). Only polychaetes (5) and benthic invertebrates (6) showed higher EE in
RNMM than in NCA while for all the other functional groups a higher EE is estimated for NCA food
web. Calculating EE excluding fishing mortality highlights a better agreement between EE estimated in
4
the two food webs (Fig. 2B, red dots), in particular for small pelagics (10), non piscivorous fishes (11),
cephalopods (8) and piscivorous fishes (12), thus evidencing similar predation mortalities going on in
the two ecosystems.
Modified Lindeman Spine for exploited and protected food web (Fig. 3) showed that Transfer
Efficiency (TE) is generally higher in the exploited ecosystem than in RNMM. Both classic food chains
of RNMM, grazing and detritus-based, show decreasing transfer efficiencies for increasing values of
TL, and TE of grazing food chain is, for any TL, higher than corresponding efficiency of detritus-based
chain. Such pattern is not evidenced in NCA food web that shows transfer between TL III and TL IV
respectively minimum in grazing food chain (TE=2.4) and maximum in the detritus-based chain
(TE=18.8). The low TE between TL III and TL IV in the grazing food chain can be related with the
high production of jellyfish and the low use of this production in the food web, while the higher TE
between TL III and TL IV in the detritus food chain can be related with the higher use of decapods and
cephalopods with TL ≈ III. Moreover, the low TE (TE=1.8) between TL II and TL III in detritus food
chain evidences the importance of benthic invertebrates in the NCA model. The TLco is 2.02 and 2.16
respectively for the detritus-based and the grazing food chain of the NCA model, while correspondent
TLco values for RNMM food chains are 2.10 and 2.38. Accordingly with this, TLco for the whole food
web (excluding TL=1) is 2.12 and 2.28 for NCA and RNMM, respectively.
Primary production that flows into detritus in RNMM food web is much higher than in NCA and this is
due to the macrobenthic producers that are less palatable than phytoplankton and thus less used within
the food web. Export in detritus is one fold higher in RNMM food web and it has to be intended as the
surplus in the mass-balance that can outflow from the system (as it is likely to occur in Miramare) or
accumulate into the bottom sediments (more likely to occur in the Adriatic large system).
Synthetic indices estimated for the two food webs are compared in Fig. 4. It has to be observed that
large differences between the two food webs are encountered for properties and indicators directly
related to primary production (i.e. Net Primary Production, Net system Production, Flows to detritus,
Production, Exports, Primary production/Respiration, Primary Production/Biomass): all these indices
are one-two folds higher in RNMM than in NCA food web. Some indices of ecosystem maturity and
stability (i.e. Biomass/throughput, Omnivory index) have similar values in the two food webs, while
Connectance Index, Biomass/Production, Finn’s path length are slightly higher in NCA food web and
Finn’s cycling index is more than double in NCA food web than in RNMM (Fig. 4).
Estimation of total effect of each functional group on the food web is reported in Fig. 5 for the two
ecosystems. In the fished ecosystem, small pelagics (10) show the highest total impact despite a
relatively low biomass and thus can be considered key functional group (Piraino et al., 2002), while an
analogous role is played in protected ecosystem by non piscivorous demersal fishes (11) and top
predators (13). Conversely benthic invertebrates (6) and primary producers have high impacts and high
biomass in Adriatic and Miramare food web respectively, thus they appear to be structuring functional
groups (Piraino et al., 2002). Jellyfish (3) and polychaetes (5) showed similar patterns in the two food
webs, appearing as groups with intermediate abundances and effects.
Results of trophic spectra analyses are shown in Fig. 6. Production spectrum (Fig. 6A) highlights the
higher production of NCA food web for all range of TL except for TL close to 3 mainly due to small
and medium sized pelagic fish production in the protected area. Conversely, spectrum of biomass over
trophic levels (Fig. 6B) shows higher biomasses in Miramare food web for all TL below 3.1. Fig. 6C
reports the ratio between the previous two spectra, thus showing the spectrum of the ratio P/B that
5
evidences an exponential decreasing trend of P/B for NCA and a more constant P/B over all TL range
for RNMM food web. Trophic spectrum of catches for Adriatic Sea (Fig. 6D) shows that exploitation is
targeting mainly species at TL close to 3, but discards are highly concentrated at TL=2.
Discussion
Comparison among the food webs of protected and fished area of the Adriatic Sea evidences a number
of differences that cannot be ascribed to fishing impacts alone. Indeed, the two food webs describe
ecosystems of different dimensions, thus while Miramare food web can be considered very local and
specific (Tempesta, 2005; Libralato et al., submitted), the North and Central Adriatic Sea food web
represents the average of a quite vast area (Coll et al., submitted). At the same time, while Adriatic
model represents the food web of the pelagic and demersal continental shelf system, Miramare food
web points toward the description of a coastal area.
As an example, modified Lindeman spine highlights the higher importance of grazing food chain than
detritus–based one in NCA food web; conversely, RNMM, due to the presence of benthic macroalgae
and seagrasses, showed large primary production that necessarily is accumulated into the detritus or
more likely exported. Moreover, the higher importance of top predators in the NCA food web in
comparison with RNMM is related with the lower dimensions of the latter, which is limited in terms of
top predator presence. On the contrary, the higher biomass and production of seabirds in Miramare
reserve is also related with the coastal nature of the area.
On the other side, the comparison highlights common patterns between food webs. For example, the
relative maximum of biomass and production spectra for TL=3 is due to the high abundance of smallmedium sized pelagic, non piscivorous and benthopelagic fishes in both food webs. Moreover, many
functional groups show similar trophic levels, highlighting similar ecological roles in both ecosystems,
and EE estimates evidence similar use of production in the two food webs if fishing mortality is
excluded.
However, despite differences inherent to the food webs features and the different amount of data used
for their description, inevitably affecting their robustness, several results evidence the effects of fishing.
For example, fishing activities imply higher use of production (higher EE) in many of the functional
groups for the NCA food web. The mean trophic level of the community (TLco), expected to decrease
in ecosystems impacted by fisheries (Rochet and Trenkel, 2003), is lower in the NCA food web than in
the protected area. Moreover, while both detritus-based and grazing food chains show lower TLco in
NCA than in RNMM, the TLco estimated for NCA grazing food chain is particularly lower than the
correspondent one in RNMM, highlighting high impact on grazing food chain in fished ecosystem.
Trophic spectra results are particularly important in evidencing a reduction in biomasses in the fished
ecosystem and highlighting higher production in the exploited ecosystem than in protected one.
Moreover P/B spectra shows that productivity in fished ecosystem is higher at low trophic levels than
in protected area, but while P/B is exponentially decreasing over TL in the former, it is almost constant
in the latter, thus P/B in RNMM are estimated higher than in NCA for high TL. These results are a
clear confirmation of the effects that exploitation has on biomasses and production patterns: decreasing
the average trophic level of the community (Pauly et al., 1998; Piet and Jennings, 2004), increasing the
productivity at low trophic levels in order to sustain high trophic levels targeted by fisheries.
6
Moreover, fishing can be very likely the cause of anomalies in transfer of energy along classical food
chains as highlighted by the modified Lindeman Spine. Food web of the protected area has a
monotonic decrease of TE for increasing TL that is in accordance with theoretical proposals
(Lindeman, 1942; Burns 1989; Strayer, 1991). Conversely, food web of the fished system provided
clearly non monotonic efficiencies: although these anomalies can be ascribed to fishing effects since
they occur at TL=III, the most exploited trophic level (mainly due to fishing of small pelagic fishes),
further investigations are needed for unambiguously identify such non-monotonic feature of TE values
as an effect of fishing. In relation to this, TL II related with detritus-based chain is also partially fished
(mainly due to fishing of benthic invertebrates) and shows very low TE from TL II to TL III,
highlighting a low use of the production of this compartment in the food web of NCA model,
production that is converted into detritus. This TL II is also maintained mainly by detritus. Therefore,
the link between the benthic invertebrates and detritus components of the NCA model is shown to be a
key interaction in the exploited food web, interaction that could be enhanced directly or indirectly by
fishing activity (e.g. due to removal of predators).
Comparison of synthetic indices for the food webs is controversial and it has been highlighted that such
comparisons seems to be useful when developed within similar ecosystems in different periods of time
rather than between different ecosystems (Jarre and Christensen, 1998; Tudela et al., 2005). However,
several indices describing both Mediterranean food webs are similar thus highlighting ecosystem type
similarities, while main differences among synthetic indices have been related with differences on
primary production data on both models.
Mixed trophic impacts analysis highlights the little impacts of cephalopods, marine turtles and
benthopelagic fishes in both food webs. Interestingly, despite their very low biomass, non piscovorous
fishes, top predators and seabirds have high impacts in the protected but not in the fished area’s food
web. Conversely small pelagics and decapods (respectively target and by-catch of fisheries) have high
impacts in NCA and intermediate impact in RNMM food web.
The high importance of small pelagics for the NCA ecosystem and fisheries is, however, due to the
high positive impacts on their predators and high negative impacts they have on benthopelagic fishes,
on small pelagics themselves and on non piscivorous demersal fishes as evidenced from the mixed
trophic impact analysis (not reported). These negative impacts have to be considered as competition for
food resources. The high impact of small pelagics on the trophic web is a feature identified also in
other ecosystems (Cury et al., 2000) and need particular attention: due to their importance (key role),
their overexploitation can bring to deep changes in structure and functioning of the ecosystem, and
therefore a precautionary approach (FAO, 1996) is needed for the management of the fisheries
targeting these species in Adriatic Sea.
Conclusions
Despite ecological and dimensional differences in the fished North and Central Adriatic and protected
Miramare Natural Marine Reserve, the comparison of their food webs is useful in highlighting
differences that can be associated to fishing activities. Results gave insights on effects of fishing on
ecosystem structure and functioning, in particular enhancing productivity and decreasing standing
stocks.
7
Considering the whole food web, both exploited and protected ecosystems seem to have similar
properties, thus evidencing a similar functioning, except for some effects related to fisheries
exploitation. This similar functioning, however, is obtained through a different role played by
functional groups within the two food webs.
Results also highlight effects of protection, in particular increasing trophic level of the community and
accounting for higher biomasses with respect to fished ecosystem. Therefore these results highlight the
usefulness of protection of marine areas as valid tool for the management of natural resources.
However, it has to be taken into account that presented results are at their preliminary stage and that the
use of dynamic models calibrated with time series of biological data can provide further evidence of the
generality of differences found between protected and non protected food webs and ascribed to fishing
effects.
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11
Standardized food web model
1
Primary producers
2
Zooplankton
3
4
5
Jellyfish
Suprabenthos
Polychaetes
6
Benthic invertebrates
7
Decapods
8
Cephalopods
9
Benthopelagic fishes
10
Small and medium-sized pelagic
fishes
11
Non piscivorous demersal
fishes
12
Piscivorous fish
13
Top predators
14
15
Marine turtle
Seabirds
16
Detritus
1
North and Central Adriatic
Phytoplankton
2
3
4
5
6
7
8
9
10
11
12
13
14
27
Micro and mesozooplankton
Macrozooplankton
Jellyfish
Suprabenthos
Polychaetes
Comm. scallops and gasterop.
Benthic inv.
Shrimps
Norway lobster
Mantis shrimp
Crabs
Octopus
Squids
Benthopelagic fishes
28
29
30
31
32
24
25
26
Anchovy
Sardine
Small pelagic fishes
Horse mackerel
Macherel
Dem. fish1
Mullets
Flatfish
15
16
17
18
19
20
21
22
23
33
34
35
37
36
38
39
40
Vul. hake
Non vul. hake
Gadids
Conger eel
Anglerfish
Turbot and Brill
Dem. fish2
Dem. sharks
Dem. skates
Small tunids
Large pelagic fishes
Dolphins
Marine turtles
Seabirds
Discards
By catch
Detritus
17
18
15
16
*
12
11
10
14
13
Miramare Reserve
Phytoplankton
Macrobenthic producers
Microzooplankton
Mesozooplankton
Jellyfish (1)
Amphipods
Polychaetes
Bivalves
Echinoderms
Decapods
(2,3)
*
Cephalopods
2
3
1
Atherina spp.
Chromis chromis
Engraulis encrasicolus
5
6
7
8
9
4
Diplodus spp.
Mugilidae
Sarpa salpa
Sciaena umbra
Sparus aurata
Dicentrarchus labrax
*
Sharks and rays
*
*
19
Marine turtles
(5)
Seabirds
Detritus
(2,3,4)
(3)
Table 1. Functional groups in the standard model identified for Mediterranean food web and
corresponding groups of the North and Central Adriatic and Miramare Reserve food webs. For
these food webs original numbering is reported (see respectively Coll et al., submitted and
Libralato et al., submitted). Miramare Natural Marine Reserve food web was complemented with
some groups (identified by *), and information available in literature: (1) Piccinetti and Piccinetti
Manfrin, 1984; Malej, 1989; Zavodnik, 1991 (2) ISMAR-CNR biological database (1990-1997);
(3) Coll et al., submitted; (4) Jardas, 1972; Capapé and Quignard. 1977; Zupanovic and Jardas,
1989; Costantini et al., 2000; (5) Fasola et al., 1989; Bogliani et al., 1992; Boldreghini et al.,
1997; Baccetti et al., 2002.
12
10000
10000
1000
1000
100
100
Invertebrates
6
Consum ers
1
2 Invertebrates
6
3
Consum ers
B Adriatic
4
0.0001
0.001
0.0113
1
0.1
8
7
1 12
9
10
11
4
5
100
1000
10000
P Adriatic
2 Fish
3 10
10
1
Fish
10
5
10
7
1
0.0001
0.001
0.01
13
12
1
0.1
8
9
11
10
100
1000
10000
0.1
0.1
14
+10000%
0.01
15
0.01
14
+ 1000%
15
0.001
0.001
+100%
A
- 90%
- 99%
B
0.0001
0.0001
P Miramare
B Miramare
Fig. 1. Comparison of biomasses (left figure, A) and productions (right figure, B) of each functional
group (black dots) and of ecological main groups (red dots), i.e., all fish, all invertebrates, all
consumers for food webs of Miramare and Adriatic. Functional groups are numbered according
with Table 1.
4,5
1
11
0,9
13
4
7
9
9
2
8
1
15
12
8
3,5
7
12
0,8
14
16
0,7
10
7
3
9 10
EE Adriatic
TL Adriatic
11
14
3
2,5
4
2
2
5
0,6
4
0,4
0,3
6
12
3
A
1,5
0,1
15 13
0
2
2,5
3
TL Miramare
3,5
4
4,5
B
5
13
1, 16
1
1,5
8
11
0,2
1
10
0,5
0
6
0,2
0,4
0,6
0,8
1
EE Miramare
Fig. 2. Comparison of trophic level, TL, (left figure, A) and ecotrophic efficiency, EE, (right figure, B)
estimated for each functional group in Miramare and Adriatic food webs. Fig. 2B also reports
estimates of EE obtained by excluding fishing mortality (red dots). Functional groups are
numbered according with Table 1.
13
Fig. 3. Modified Lindeman Spine for the trophic web of fished ecosystem (above) and protected area
(below). Roman numbers stand for integer trophic levels, P for Primary Producers and D for
detritus, thus are identifiable classic detritus-based and grazing food chains. Flows are in gww m2
year-1 and biomasses in gww m2 .
14
10000
Throughput
Consumption
Production
Net Primary Prod.
Respiration
Flow s to detritus
Exports
Biomass
System Indices - Adriatic
1000
100
Ascendency %
Finn's Cycling Index
Net system Production
10
+10000%
Finn's Path Lenght
Primary Prod/Biomass
Respiration/Biomass
Primary Prod/Respir
1
0,01
+1000%
0,1
1
10
100
1000
10000
Connectance Index
Omnivory Index
Biomass/Production
0,1
+100%
Biomass/Throughput
-50%
-90%
0,01
-99%
Syste m Indices - M iramare
Fig. 4. Comparison of synthetic indices estimated for the food webs of protected (Miramare Reserve)
and exploited (North and Central Adriatic) ecosystems. Indices are represented in logarithmic
scales in order to compare their ranging over some orders of magnitude.
15
1,0
11
10
1
13
6
2
7
0,8
1
15
0,6
12 2
Total effect
10
0,4
11
5
8
12 4
7
5
3
3
0,2
13
9
Primary producers
Zooplankton
Jellyfish
Suprabenthos
Polychaetes
Benthic invertebrates
Decapods
Cephalopods
Benthopelagic fish
Small and medium-size pelagic fish
Non piscivorous demersal fish
Piscivorous fish
Top predators
Seabirds
Marine turtles
Miramare food web
9
8
0,0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Adriatic Sea food web
14
15
14
4
0,0
0,2
Biomass proportion
Fig. 5. Effect of each functional group on all the other groups of the food web estimated for Miramare
and North Adriatic standardized food webs. Groups are numbered according with Table 1. Two
groups showed high effect and high biomass (structuring functional groups) and are out of scale,
i.e., Phytoplankton for Miramare food web (biomass proportion = 0.74; total effect=0.96) and
Benthic invertebrates for Adriatic food web (biomass proportion =0.61; total effect = 0.93).
16
3
20
A
18
Adriatic Sea
B
Miramare
Adriatic Sea
Miramare
Deleted: A
2.5
14
Biomass (gww m -2)
Production (gww m -2 year -1)
16
12
10
8
2
1.5
1
6
4
0.5
2
0
0
2
2.2
2.4
2.6
2.8
3
3.2
3.4
2
2.2
2.4
Trophic Level
2.6
2.8
3
3.2
3.4
Trophic Level
30
0.14
P/B Adriatic Sea
C
D
P/B MIramare
Discards
Deleted: C
Landings
25
year -1)
0.12
0.1
-2
Catches (gww m
P/B (year -1)
20
15
10
0.08
0.06
0.04
5
0.02
0
0
2
2.2
2.4
2.6
2.8
Trophic Level
3
3.2
3.4
2
2.2
2.4
2.6
2.8
3
3.2
3.4
Trophic Level
Fig. 6. Analysis of trophic spectra for production (A), biomasses (B) and production/biomass (C) for
food webs of protected (Miramare) and exploited ecosystem (Adriatic Sea). P/B is estimated by
the ratio of trophic spectra of production and Biomass. Trophic spectra of catches (D) for
Adriatic food web is reported for landings and discards.
17

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