Hydrobiologia (2013) 717:85–108

DOI 10.1007/s10750-013-1576-8

PRIMARY RESEARCH PAPER

Structure and functioning of two pelagic communities

in the North Chilean Patagonian coastal system
Héctor J. Pavés • Humberto E. González •

Villy Christensen

Received: 7 July 2012 / Revised: 15 May 2013 / Accepted: 25 May 2013 / Published online: 19 June 2013
Ó Springer Science+Business Media Dordrecht 2013

Abstract The size composition of primary produc-
ers is important for how energy is channeled through a
food web and on to the higher trophic levels and
eventually to fisheries. To evaluate this, we studied the
productive patterns for large (micro) versus small
(nano) phytoplankton in two south marine Patagonian
ecosystems: The Inner Sea of Chiloe—ISCh and,
Moraleda Channel—MCh. We built Ecopath models
Handling editor: Mariana Meerhoff
Electronic supplementary material The online version of
this article (doi:10.1007/s10750-013-1576-8) contains
supplementary material, which is available to authorized users.
H. J. Pavés  H. E. González (&)
Instituto de Ciencias Marinas y Limnológicas, Facultad de
Ciencias, Universidad Austral de Chile, Valdivia, Chile
e-mail: hgonzale@uach.cl
H. J. Pavés
Fisheries Centre, University of British Columbia,
Vancouver, BC, Canada
H. E. González
COPAS Sur Austral (PFB-31/2007) and COPAS,
Center of Oceanography, Universidad de Concepción,
Concepción and Patagonian Ecosystem Research Center
(CIEP), Coyhaique, Chile
V. Christensen
Fisheries Centre, University of British Columbia,
Vancouver, BC, Canada
(EwE), and evaluated the hypothesis that the overall
primary productivity—rather than the ratio of large to
small primary producers—constitutes an adequate
proxy for predicting the amount of secondary and
tertiary production and biomass (up to the fisheries).
The EwE model included four small-scale fisheries
and 36 functional groups. The functioning of both
ecosystems was similar but the ecosystem parameters
(biomass, energy transfer efficiencies from primary
producers, secondary, and tertiary production) were
twice as much in the basin with more microphyto-
plankton biomass. Overall, the hypothesis was
rejected, albeit it was possible to highlight the
importance of the quality and size spectrum of
plankton on the structure of marine ecosystem, and
to demonstrate the key role of the microbial loop over
traditional food web in the functioning of the carbon
biological pump in Patagonia ecosystems.
Keywords Ecopath  Microbial loop  Traditional
food web  Patagonian coastal system
Introduction
Comparisons of the planktonic community structure
and ecosystem properties have shown considerable
biomass differences between different pelagic sys-
tems, irrespective of primary productivity (PP) rates
(Peña et al., 1990; Smith et al., 2001; Pavés &
González, 2008; Pavés et al., unpublished data). Such

123
86
differences in PP may affect secondary production,
which, due to bottom-up effects on the food web, may
then impact tertiary production including fisheries,
e.g., changes registered under El Niño conditions in
the Pacific Ocean (Iriarte & González, 2004; Escrib-
ano et al., 2004; Mattern et al., 2004; Oliveira et al.,
2006; Arcos et al., 2001, 2004). Another important
feature is when the microphytoplankton/nanophyto-
plankton biomass ratio is[1, the levels of biomass are
higher than when this ratio is\1. These characteristics
hold true on different temporal (winter: nanoph-
dominated versus spring: microph-dominated) and
spatial scales (coastal: microph-dominated versus
oceanic: nanoph-dominated) (Peña et al., 1990; Iriarte
& González, 2004; González et al., 2010, 2011). Thus,
the environments with high biomass levels for primary
producers are also characterized by high levels of
secondary and tertiary production.
In order to understand the relationship described
above, the different parts of the pelagic community,
considering all groups from bacterioplankton to mam-
mals and fisheries, must be described within a single
model. Computational tools such as Ecopath with
Ecosim (EwE; Christensen & Pauly, 1992; Pauly et al.,
2000; Christensen et al., 2008; Christensen & Walters,
2011) can be used to analyze and simulate trophic
subwebs and to determine the amounts of biomass and
fluxes of matter for the different trophic levels.
Herein, we use EwE to study the trophic relation-
ships and energy flows among different parts of the
trophic web (EwE v 6.0; Christensen et al., 2000,
2008; Pauly et al., 2000; Christensen & Walters,
2004), impacted with different levels of fishery
pressure in the Chilean North Patagonian pelagic
ecosystem. This study aims: (1) To determine the
ecosystem properties, biomass levels, and energy
flows of the pelagic community in the studied systems,
and to evaluate the relationship between PP and the
producer’ biomasses; and (2) To determine differences
in the functioning of these pelagic food webs between
the ecosystems under evaluation. We tested the
hypothesis that PP measured in different marine
systems constitutes an adequate proxy for predicting
the amount of secondary and tertiary production (up to
the fisheries level) in coastal marine systems, fjords,
and channels. In addition, irrespective of the PP, when
the energy flows through the classical food web (i.e.,
large-sized phytoplankton and mesoplankton), differ-
ences in the ecosystem functioning and higher level in
123
Hydrobiologia (2013) 717:85–108
secondary and tertiary productivity/biomass and fish-
ery activities can be observed than when the energy
flows through the microbial food web (channeling
through nano- and picoplankton).
Materials and methods
Models were built for two semi-enclosed basins of the
Chilean Patagonia, Inner Sea of Chiloé (ISCh) and
Moraleda Channel (MCh) (Fig. 1). Topographically,
these two areas are different: ISCh is considered to be
an inner sea because of its wide connection with the
ocean and great basin size, whereas MCh is a channel–
fjord system (Silva & Palma, 2008) with a more
restricted connection to the ocean. The ISCh form a
basin *11,000 km2 and with an average depth of
250 m and receives freshwater from different rivers
(Davila et al., 2002). The ISCh basin is connected
to the Pacific Ocean through two channels: Chacao
(*2 km wide) and Corcovado (*30 km wide). The
latter offers the most important area for the exchange of
water masses with the ocean (Palma & Silva, 2004).
Thus, a great part of the ISCh is influenced by Sub
Antarctic Water (SAAW) and Sub Antarctic Modified
Water (SAMW), salty water masses that contribute
macronutrients from the ocean (Palma & Silva, 2004).
On the other hand, MCh, is a basin of *4,100 km2 and
has an average depth of 230 m with a smaller water
exchange with the ocean than the ISCh. The MCh basin
is connected to the ocean by a series of 11 transversal
channels (*2 km wide) and the Corcovado Gulf
(*19 km wide) at the northern end of the basin.
Freshwater input enters to the MCh from different
fjords, estuaries, and glaciers (Davila et al., 2002). The
shallowest portion of the MCh is located close to the
Minenea Constriction-Sill, a natural barrier that pre-
vents the entrance of nutrient-rich SAAW below
150 m, and the dominance of Estuarine Water (EW),
which is rich in silicic acid and has lower salinity and
nutrient concentrations than the oceanic water (Palma
& Silva, 2004). These topographical differences have
been linked to their biomass differences: ISCh has
more biomass of primary and secondary producers
than MCh (Pavés et al., unpublished data), however,
the PP at the ISCh (786 mg C m-2 d-1) is slightly
lower than at the MCh (947 mg C m-2 d-1) (annual
averages obtained for the same area considered in this
research; González et al., 2010, 2011).
Hydrobiologia (2013) 717:85–108 87

Fig. 1 Study area in the

Chilean Patagonian fjords
and channels region,
showing the two contrasted
basins: Inner Sea of Chiloé
(ISCh, 41–43°S) (upper
panel) and Moraleda
Channel (MCh, 43–46°S)
(bottom panel). The black
circles show the sampling
sites for organisms from the
microbial and traditional
food webs

For modeling, we used information from the two
most contrasting seasons (winter and spring), thereby
covering the seasonal variability in the annual aver-
ages. The 36 functional groups used were those with
enough data available for the studied area. Emphasis
was placed on the role of the microbial (i.e.,
picoplankton, nanoplankton, microplankton) and tra-
ditional food webs (i.e., mesoplankton, megaplankton,
nekton, marine mammals, seabirds) and the more
important fisheries activities in each basin. The
microbial loop and mesoplankton data for ISCh and
MCh, were collected during 2006–2007. The mega-
plankton was collected during 2005–2007, the nekton
during 2005–2008, the seabirds during 2008, the
marine mammals during 1998 (sea lion) and 2009
(cetacean). And the fisheries activities information and
their resources were obtained for the 2003–2009
period (Annex 1, 2, 3).
The groups considered were: (1) Otariidae (Otaria
flavescens, Arctophoca australis gracilis); (2) Aves
(Thalassarche melanophrys, Puffinus griseus, Pelec-
anus thagus, Spheniscus humboldti, Spheniscus mag-
ellanicus, Phalacrocorax atriceps, Phalacrocorax
magellanicus, Phalacrocorax gaimardi); (3) Orcinus
orca; (4) Mysticeti (Balaenoptera musculus, Balae-
noptera acutorostrata, Megaptera novaeangliae,

123
88
Balaenoptera physalus, Eubalaena australis); (5)
Delphinidae (Cephalorhynchus eutropia, Lagen-
orhynchus australis, Tursiops truncatus); (6) Gem-
pylidae (Thyrsites atun); (7) Sciaenidae (Cilus
gilberti); (8) Atherinopsidae (Odontesthes regia); (9)
Ophidiiformes (Genypterus chilensis, Genypterus bla-
codes, Genypterus maculatus); (10) Gadiformes adult
(Merluccius australis, Micromesistius australis, Ma-
cruronus magellanicus); (11) Gadiformes juvenile-
larvae; (12) Carangidae (Trachurus murphyi); (13)
Clupeiformes adult-juvenile (Sprattus fuegensis,
Strangomera bentincki, Engraulis ringens); (14)
Clupeiformes larvae; (15) Ichthyoplankton; (16)
Scyphomedusae (Chrysaora plocamia); (17) Hydro-
medusae (Soltmtndetla hitentacittata, Ciytia simplex,
Amphogona apicata, Bougainvillia macloviana); (18)
Ctenophora (Pleurobrachia bachei); (19) Appendicu-
larians (Oikopleura dioica, Oikopleura longicauda);
(20) Siphonophora (Lensia conoidea, Muggiaea at-
lantica, Sphaeronectes gracilis); (21) Salpida (Salpa
fusiforme, Thalia democratica); (22) Decapoda larvae
(Neotrypaea uncinata, Sergestes articus, Munida
subrugosa); (23) Euphausiacea (Euphausia vallentini,
Nematoscelis megalop); (24) Chaetognatha (Sagitta
tasmanica, Sagitta marri, Eukrohnia hamata, Sagitta
gazellae); (25) Cladocera (Podon leuckarti, Evadne
nordmanni, Pseudevadne tergestina); (26) Copepoda
calanoida (Calanus australis, Calanoides patagonien-
sis, Drepanopus forcepatus, and copepods [
800 lm); (27) Copepoda cyclopoida (Oithona similis,
and copepods \ 800 lm); (28) Copepoda nauplii;
(29) Ciliophora (ciliates); (30) Microphytoplankton
(diatoms, autotrophic flagellates); (31) Microflagel-
lates (heterotrophic dinoflagellates); (32) Heterotro-
phic nanoflagellates (HNF); (33) Autotrophic
nanoflagellates/nanophytoplankton (ANF); (34) Bac-
teria (picoplankton); (35) Dissolved organic matter
(DOM—detritus); and (36) Detritus—particulate
organic carbon (POC) (Annex 1).
Ecopath with Ecosim provides mathematical models
at the static and dynamic ecosystem-levels (EwE;
Christensen et al., 2008; Pauly et al., 2000; Christensen
& Walters, 2011). EwE produces trophic ecosystem
models that are mass- and energy-balanced, for a
nonsteady-state, and allow the input of a variable
number of functional groups and fishing fleets. All of
these are connected through physiological and ecolog-
ical linear equations that describe the ecosystem features
(Ecopath module) or predict variations in the biomass of
123
Hydrobiologia (2013) 717:85–108
their components, either along temporal (Ecosim mod-
ule) or temporal-spatial (Ecospace module) dimensions
(Christensen et al., 2000, Christensen & Walters, 2004;
Pauly et al., 2000, Walters et al. 1999).
The EwE software uses a system of concurrent
linear equations based on ecological assumptions,
connecting the different functional groups and fisher-
ies in a multi-taxa model. The model assumes mass
balance within the system over the study period (in this
case, averaged over 1 year) such that the production of
any prey is equal to the biomass consumed by the
predators plus any other use of production within or
exported from the system, and was expressed by the
equation:
Bi  ðP=BÞ  EEi ¼ R Bj  ðQ=BÞj DCij þ Yi þ Exi
þ BAi ð1Þ
where Bi and Bj are the biomass of prey and predator,
respectively; (P/B)i is the production/biomass ratio;
EEi is the ecotrophic efficiency that corresponds to the
fraction of the production consumed (or caught) within
the system with the remaining fraction going to
detritus; (Q/B)j is the food consumed per unit biomass
of predator j; DCij is the proportion of prey i in the diet
of predator j; Yi is the fish catch rate; and Exi is other
export (e.g., net migration); BAi is the biomass
accumulation rate for i (Christensen et al., 2000).
The input data for these models were B, DC, P/B, and
Q/B, using the B, P, Q, and DC data available for the
study area and from the literature (for references and
periods considered see below, and Annex 1). The B
values were expressed as mg C m-2; P and Q values as
mg C m-2 year-1; and P/B and Q/B as year-1. The
daily Q/B and P/B ratios for the plankton groups were
multiplied by 365 to obtain annual rates (Annex 1).
Data on fish catch rates (Y) were annual and expressed
as mg C m-2 year-1. Migrations (E) were not consid-
ered in this study, i.e., they were assumed to be zero.
We assumed that our study system was in a steady state
(sensu Christensen et al., 2000) and that its populations
were in equilibrium (sensu Allen, 1971; in Christensen
et al., 2000). This implies that the biomass accumula-
tion (BA, mg C m-2 year-1) rates were assumed
to be zero.
For biomass data of microbial loop and zooplank-
ton species, we pooled the information from the
springs and winters of 2006 (cruise CIMAR 12-Inner
Sea of Chiloe), and 2007 (cruise CIMAR 13-Moraleda
Hydrobiologia (2013) 717:85–108
Channel) to obtain an annual mean. All cruises were
conducted on board the AGOR ‘‘Vidal Gormáz’’ of the
Chilean Navy. For biological data of zooplankton
species, we used information from the literature (see
Annex 1). For biomass and biological data of the
traditional food web parts, we pooled the seasonal
information from the fisheries reports of SERNAPesca
(www.sernapesca.cl) and Fondo de Investigación
Pesquera (www.fip.cl), as well as other published
information on seabirds and marine mammals (see
Annex 1). The Clupeiformes and Gadiformes biomass
([80% of total regional landings) were obtained from
stock assessments in each study area (see Annex 1).
Other fish resources (e.g., Gempylidae, Sciaenidae,
Atherinopsidae, Ophidiiformes, Carangidae) for
which little information was available and that repre-
sented low biomass landings (\20%) were included
only as a first evaluation of their potential ecological
(trophic) impact in the studied sub-food webs.
We estimated the diet composition for each group
using different approaches, but all were expressed as
frequency of weight (WF%): (a) from the frequency
of occurrence or number of the prey in the guts
multiplied by carbon weight (e.g., Clupeiformes,
Chaetognatha, Euphausiacea, Ctenophora); (b) from
experiments on ingestion rates conducted in the
studied areas (for Copepoda, Appendicularia, Salp-
ida); and (c) from other carbon models (Flagellata,
Ciliophora, see Annex 1, 2). Predation on Copepoda
cyclopoida, Copepoda calanoida, and Cladocera was
estimated according to bibliographic information.
However, in those cases in which the diet information
did not differentiate between these crustacean classes
(for half of the copepod predators), predation on
copepods and cladocerans was estimated according to
the in situ availability of each one, assuming no
predator selectivity (e.g., Salpida, see Vargas &
Madin, 2004) (Annex 2). This constituted an over-
simplification of the model that should be improved
by including new empirical data on diet composition,
abundance, and selectivity from the studied areas.
Although mechanical selection of large over small
prey might be possible in small pelagic fishes and
euphausiids, for purposes of simplification (and
because very little information is available on this
issue), we did not consider this possibility. The
contributions of DOM and detritus from each func-
tional group were obtained from published informa-
tion (see Annex 2).
89
The artisanal (small-scaled fisheries) landings of
the most important pelagic fishes (Clupeiformes
purse-seine on Clupeiformes species, gillnet fishery
on Sciaenidae and Atherinopsidae, mackerel purse-
seine on Carangidae, line hand fishery on Gempylidae)
and some deep-sea species (Long line fishery on
Ophidiiformes and Gadiformes) in the study area were
obtained from the ‘‘Anuario Estadistico de Pesca’’,
National Agency of Fisheries (Servicio Nacional de
Pesca; www.sernapesca.cl). This fishing fleet is
formed by vessels among 6–15 m length and until
80 ton of storage capacity. The data input were an
average of 5 years (2003, 2006, 2007, 2008, 2009)
(Annex 3). Fish discard biomasses were obtained from
stock evaluation and discard reports (see Annex 1, 3).
Biomasses of top predator discards were obtained
from publications or reports about operational inter-
actions between marine mammals, seabirds, and fish-
eries realized in or near the studied areas (see Annex
1). The fate of the discarded fishes was assumed to be
50 % of detritus (POC), 49.9 % of export of pelagic
system and 0.1 % of DOM.
The EwE model required a balance between the
input and output of energy for all functional groups.
This balance was expressed by means of the linear
equation described by Winberg (1956; see Christensen
et al., 2000), which assumes that the material
consumed by one organism (Q) corresponded to the
sum required by the individual for somatic and
gonadic growth (P), metabolic costs (R), and the
production of organic waste or non-assimilated food
(UF) (Christensen et al., 2000).
To determine the trophic level of each functional
group considered, we applied the theoretical formu-
lation of fractional trophic levels by Odum and Heald
(1975). Trophic level one (TL1) corresponded to
primary producers and detritus. Consumers were
located in trophic level 1? the weighted average of
the prey’s trophic level (Christensen et al., 2000).
For both models and when required, we adjusted
the original data of B, P/B, and Q/B until obtaining
mass- and energy-balanced models. When the respi-
ration (R) of a functional group was negative, we
increased the ingestion rate values until reaching a
value of R giving about 0.5 R/Q (Christensen et al.,
2000). If the EE of a functional group was [1,
modifications in the B, P/B, Q/B, and DC were made
using bibliographic information about life histories of
the species (e.g., average life span, age at first sexual
123
90
maturity, stock evaluation, behavior data; see
Annex 1). The modifications in P/B and Q/B were
done until the P/Q ratio was 0.001 to 0.100 for marine
mammals and seabirds, 0.100 to 0.300 for fish groups,
0.200 to 0.400 for macro and mesoplankton groups,
0.300 to 0.500 for nano- and microplankton groups,
and [0.500 for the picoplankton group (bacteria). To
make these changes, we sought to adjust values from
the literature so as to be physiologically acceptable for
each species (Christensen et al., 2000). In normal
cases, P/Q values ranged from 0.05 to 0.3, i.e., the
consumption of most groups was about three to ten
times higher than their production (Christensen et al.,
2000). Exceptions were top predators, e.g., marine
mammals, which could have lower P/Q values, and
small fast-growing fish larvae, nauplii, or bacteria,
which could have higher P/Q values (Christensen
et al., 2000).
The B of the poorly represented zooplankton
groups in the samples were increased between two
and 300 times depending on the group, with the
respective extremes being Copepoda and Salpida. This
increase was based on the fact that vertical hauls with a
zooplankton net usually underestimate the abundance
of small-sized zooplankton and gelatinous plankton
groups like Cladocera, Salpida, Copepoda cyclopoida,
Chaetognatha, Siphonophore, Scyphomedusae, and
Ctenophora (Gallienne & Robins, 2001; Giesecke &
González, 2004; Stehle et al., 2007; Antacli et al.,
2010; Riccardi, 2010). In addition, these modifications
were made in order to obtain EEs \1 for each group,
and thus, reach the criteria of mass balance (Chris-
tensen et al., 2000).
We obtained a table of pedigree data that could be
used to evaluate the precision of the information
(Annex 4). Also, we obtained output to describe the
matter and energy flows and the ecological relation-
ships between all the functional groups evaluated in
the ISCh and MCh basins. The following additional
estimates were made in order to describe the func-
tioning of the trophic food web in each ecosystem: (1)
Trophic overlap index (TOI): The index values range
from 0 to 1, a value of 0 indicate that the two species
do not share resources, 1 indicates complete overlap,
and intermediate values show partial overlap in
resource utilization (Christensen et al., 2000). (2)
Mixed trophic impacts: This analysis allowed a
description of the direct (i.e., predator–prey) and
indirect (e.g., cascade effect) trophic relationships
123
Hydrobiologia (2013) 717:85–108
among the different groups of the system (Christensen
et al., 2000). A positive effect of a prey on a predator
would indicate that an increment in the prey biomass
may result in an increment in the predator biomass. In
line with this, a negative effect of a predator on a prey
would indicate that an increment in the predator
biomass may result in a decline in the prey biomass.
Thus, the effect depended on the biomasses of both
predator and prey (Christensen et al., 2000). The
estimation of these impacts was based on the differ-
ences between the average values of all trophic impact
generated by all functional groups for each ecosystem.
These values exclude the impact generated by those
groups that did not impact the functional group under
analysis (i.e. those that were not prey nor predator). (3)
Keystoneness index (KS): Keystone species are
defined as those having a relatively low biomass and
a disproportionate structuring role in the food web.
This parameter was estimated from the network mixed
trophic impact analysis described above. This param-
eter was related to the biomass of the same species
(function KS, from relation between biomass propor-
tion and overall effect on food web) (Libralato et al.,
2006). For the characterization of the ecosystem size
were used; (1) Flow to the detritus: For each group, the
flow to the detritus consisted of what was egested (i.e.,
percentage of non-assimilated food relative to food
consumption) and those elements of the group that
died due to old age, diseases, etc. (i.e., sources of
‘other mortality’, expressed by 1 - EE). The flow to
detritus was expressed as mg C m-2 year-1 and
should be positive for all groups. (2) Summary of
parameters of the analyzed system: Based on Odum
(1969) and applying EwE, it was possible to estimate
parameters that allowed an analysis of the size of a
system (Christensen, 1995). The size of any ecosystem
was characterized for the sum of all consumption,
exports, respiration flows, flows to detritus, total
system throughput, total primary production, net
system production, biomass, and total catches (Chris-
tensen, 1995). (3) The energy transfer efficiencies
(ETE): Based on the flows and biomasses, the transfer
efficiencies between successive discrete trophic levels
were calculated as the ratio between the sum of the
exports from a given trophic level, plus the flow that is
transferred from one trophic level to the next, and the
trophic level throughout (Christensen et al., 2000).
The discrete trophic levels were estimated sensu
Lindeman (1942) in Ecopath with Ecosim.
Hydrobiologia (2013) 717:85–108
Results
Ecosystem Functioning
The application of EwE allowed us to characterize the
trophic energy flows and amount of biomass in the
pelagic realm, identifying in both ecosystems under
observation four important pathways through the
micro-, meso-, and macro-plankton (both chitinous
and gelatinous zooplankton), nekton (fishes), and
meganekton (marine mammals) in both ecosystems
(Fig. 2). These important pathways started in micro-
phytoplankton (diatoms), nanophytoplankton (auto-
trophic nanoflagellates, ANF), DOM groups linked to
picoplankton (bacteria), and the detritus (POC)
(Fig. 2).
The first pathway started from microphytoplankton,
which is grazed down by micro- (copepod nauplii,
ciliates), meso- (copepods), and macrozooplankton
(euphausiids, decapod larvae). The second started
from nanophytoplankton (ANF), which is heavily
grazed down by micro- (microflagellates, copepod
nauplii, ciliates) and mesozooplankton (appendicular-
ia, salpida, copepods) and receives less pressure from
macrozooplankton (euphausiids, decapoda larvae).
The third pathway started from DOM, which flows
through bacteria and nano- (heterotrophic nanoflagel-
lates, HNF) to micro- (microflagellates, ciliates) and
mesoplankton (Cladocera). All these pathways linked
micro- and mesozooplankton to fishes and top preda-
tors. Among plankton groups, all pathways occupied
the Copepoda calanoida, Euphausiacea, and Decapoda
larvae as linking pathways toward fishes and marine
mammals (mainly baleen whales). Among fish groups,
the Clupeiformes act as connectors between the
plankton and larger nekton, and Gadiformes act as a
link toward top predators such as marine mammals
(Fig. 2). In addition, in both food webs, the jellyfish
groups (Siphonophore, Ctenophora, Hydromedusae,
Scyphomedusae) consumed the same preys as fish, a
situation that under limiting resource condition could
result in competition (e.g., Euphausiacea, Cop. calan-
oida, Decapoda larvae; Fig. 2).
Niches overlap analysis
The above-mentioned pathways allowed us to deter-
mine the characteristic overlap index between the
different functional groups of the sub-trophic webs in
91
the North Patagonian System. In the ISCh, Clupeifor-
mes larvae and Ichthyoplankton, Ichthyoplankton and
Siphonophora, Ichthyoplankton and Ctenophora, and
Clupeiformes larvae and Ctenophora showed a high
overlap of the index of predators and preys, with their
niche overlap value being close to 1 ([0.70) (Fig. 3).
In the MCh, the niche overlap index was[0.7 for these
same groups, but niche overlaps were also registered
between Gadiformes juvenile-larvae and Siphonopho-
ra, Gadiformes juvenile-larvae and Clupeiformes
adult-juvenile, Copepoda cyclopoida and Cladocera,
and Gadiformes adults and Clupeiformes adult-juve-
nile (Fig. 3).
Mixed trophic impact analysis
In general in both models, Euphausiacea positively
affected the Mysticeti (baleen whale) (Fig. 4E) and
Scyphomedusae negatively impacted the larvae fish
group, its food item (Fig. 4F). In addition, a negative
effect of one group on itself (higher intra- than inter-
group competition for resources or cannibalistic
behavior) is observed for Gadiformes (Fig. 4I), Otarii-
dae (Fig. 4J), Aves (Fig. 4K), and O. orca (Fig. 4L).
Indirect effects can be detected for microphytoplank-
ton (Fig. 4C), which had a negative effect on the
biomasses of HNF and ANF but a positive effect on
the microflagellates because the latter group predates
moderately on microphytoplankton but strongly on
nanoflagellates (both HNF and ANF; Fig. 4). The
bacteria in these ecosystems had a positive impact on
their predators, the microbial loop species, and a
negative impact on their unique food source, the DOM
reservoir; however, bacteria had a very strong intra-
specific effect (Fig. 4A).
The ANF positively impacted the zooplankton
group and, in turn, higher trophic levels (i.e., fishes
and top predators), and even produced an increase in
fishery activities (Fig. 4B). Microphytoplankton pro-
duced the same effect as ANF on these groups, but this
effect was 57–64 % stronger on the fishes, marine
mammals, and fisheries than ANF (Fig. 4C). Thus,
microphytoplankton would had a stronger impact on
ecosystem productivity and showed more efficient
trophic flows than ANF. A similar situation was
determined with Copepoda calanoida and Euphausi-
acea: the positive impact of Euphausiacea on higher
trophic levels (including fisheries) exceeds that of the
copepods by a 65–91 % (Fig. 4D, E).
123
92
Fig. 2 Trophic pathways between groups of the traditional and
microbial pelagic food webs that represent the annual average
community flows of the two basins in the Chilean Patagonian
coastal system: A Inner Sea of Chiloé (41–438S), and B Moraleda
Channel (43–468S). The thickness of the lines is proportional to
the magnitude of the energy flow between functional groups. Only
flows[0.5% are depicted in the figure. The size of the nodes are
comparable between the different functional groups of the same
model. Otar = Otariidae; Aves; O. orca = Orcinus orca;
Mys = Mysticeti; Delph = Delphinidae; Gemp = Gempylidae;
Scian = Sciaenidae; Athe = Atherinopsidae; Ophi = Ophidii-
formes; Gad (A) = Gadiformes adult; Gad (J-L) = Gadiformes
On the other hand, the jellyfish groups (Scyphome-
dusae, Siphonophora) had a negative impact mainly on
the fish larvae group (Clupeiformes larvae and
Ichthyoplankton), potential competitors (other jellies),
and jellyfish prey (e.g., Decapoda Larvae, Cladocera,
Copepoda), but they did not show intraspecific
impacts (Fig. 4F, G). The Clupeiformes and Gadifor-
mes had a positive impact on all top predator species
123
Hydrobiologia (2013) 717:85–108
juvenile-larva; Caran = Carangidae; Clup (A) = Clupeiformes
adult-juvenile; Clup (J-A) = Clupeiformes larva; Ichthyo
(L) = Ichthyoplankton; Scypho = Scyphomedusae; Hydro =
Hydromedusae; Cteno = Ctenophora; Appe = Appendiculari-
ans; Sipho = Siphonophora; Salp = Salpida; Deca (L) = Deca-
poda larvae; Euph = Euphausiacea; Chaeto = Chaetognatha;
Clado = Cladocera; C. cal = Copepoda calanoida; C. cyclo =
Copepoda cyclopoida; C. nauplii = Copepoda nauplii; Cilio =
Ciliophora; Mphyto = Microphytoplankton; Mflage = Micro-
flagellates; HNF = Heterotrophic nanoflagellates; ANF = Auto-
trophic nanoflagellates; Bacteria; DOM = Dissolved organic
matter (detritus); Detritus = particulate organic carbon (POC)
(seabirds, marine mammals) and the fisheries
(Fig. 4H, I). However, both these species showed a
strong intraspecific impact. In Gadiformes, this intra-
specific control-effect was twofold higher than in
Clupeiformes (Fig. 4H, I). Finally, all top predators
(e.g., Aves, Otariidae, and O. orca) produced a
negative impact on their different fish prey groups,
potential competitors (e.g., seabirds on carnivorous
Hydrobiologia (2013) 717:85–108
1,0
27:28
0,9
10:13
Prey overlap index
10:13
0,8 11:14
12:13
0,7
11:18
23:26
0,6
23:26
0,5
28:29
19:22
11:13
11:20
0,4
0,3
0,4 0,5
Predator overlap index
Fig. 3 Trophic overlap level among the groups of the pelagic
sub-web of the Inner Sea of Chiloe (ISCh) and the Moraleda
Channel (MCh). Only groups with an overlap index higher than
0.4 are shown (0 = without overlap, 1 = total overlap). The
functional groups are numbered as in Table 1, where numbers in
bold and cursive correspond to ISCh and MCh, respectively
fishes, O. orca on Mysticeti whale), and fisheries
catches. But these entire top predator groups had an
important intraspecific effect (Fig. 4J–L).
Despite of this general trend described in the
trophic impact, it was possible to indeed observe
difference and similarities between models. For
example, changes in bacteria and ANF biomasses
produced the same (or similar) impact on both the
ISCh and MCh food webs. But, in the others high
trophic level groups this trophic impact is higher in the
ISCh’s predators than preys, or higher in MCh’s preys
than predators (microphytoplankton, Copepoda calan-
oida, Euphausiacea). The jellyfish trophic impact was
stronger for the ISCh’s (*20–90 %) than MCh food
webs. On the other hand, change in the biomass of
Clupeiformes and Gadiformes, affected mainly the
MCh than the ISCh fisheries activities (*15–100 %).
In addition, changes in top predators’ biomass would
affect mainly their prey and the fisheries, being more
intense this effect in the MCh than in the ISCh
(*50 %).
Keystoneness index
In the ISCh and MCh ecosystems, the Scyphomedu-
sae, Hydromedusae, Copepoda calanoida, O. orca and
Ichthyoplankton were estimated to be the groups with
high keystoneness indexes (Fig. 5).
93
14:15
Ecosystem size
14:15
29:31
29:31
19:26
14:20
15:20
14:18
15:20 Flow to the detritus and biomass
25:27
25:27 11:13
14:18
15:18 25:27
11:15
15:18
10:13 Other aspects that showed us some differences
18:20 between these two ecosystems are related to the
10:11
18:20
1:5 amount of matter that flows from the different
functional groups to the detritus. In ISCh and MCh,
10:11
19:23
the total planktonic and nektonic organisms produced
19:23
18:22
*699 and 376 g C m-2 year-1 of detritus, respec-
17:21 tively, of which 63 and 59 % were in the form of DOM
0,6 0,7 0,8 0,9 1,0 and the rest was POC (Fig. 6).
The microbial loop (ciliates, microflagellates, nano-
flagellates, bacteria) produced 31 (ISCh) and 23 %
(MCh) of this detritus, mainly as dissolve excretion
(DOM) products. In these systems, the microphyto-
plankton produced 65 and 70 % of the detritus, i.e.,
*234 and 137 g POC m-2 year-1 as phytodetritus
and *216 and 126 DOM g C m-2 year-1 as exu-
dates, respectively (Fig. 6).
In the ISCh and MCh, the average annual detritus
(POC, DOC) production by the chitinous and gelati-
nous zooplankton was 3–4 and 1–2 %, respectively.
Thus, chitinous zooplankton produced 8 and 6 POC
g C m-2 year-1 and 11 and 9 DOM g C m-2 year-1
in these two systems. On the other hand, gelati-
nous zooplankton produced between *7 and 5 g
POC m-2 year-1 and * 2 g DOM m-2 year-1 in
the MCh and ISCh, respectively (Fig. 6).
The fish groups and top predators produced only
*1 and *0.006 % of the detritus in the both
ecosystems (mainly POC detritus), i.e., the fishes
produced *6 and 4 POC g C m-2 year-1 and the top
predators produced *39 and 45 POC mg C m-2
year-1 in ISCh and MCh, respectively (Fig. 6). This
means that microphytoplankton contributed 90 % of
the total POC, the micro- and mesoplankton groups
added 7 %, and the nekton (fish, top predators)
contributed 3 % in these ecosystems. Microplankton
also produced 49 and 56 % of the DOM in ISCh and
MCh, and the pico- and nanoplankton were responsi-
ble for 46 and 38 % of this total DOM.
In the MCh, the biomass was greater than in the
ISCh by 11–19 times for top predators (cetaceans), 1.5
for Gadiformes, 1.4 for Hydromedusae, and 2.6 for
Copepod nauplii. However, in the ISCh, the total
biomass is *1.5 times more than in the MCh (13.5 vs.
8.9 g C m-2; Tables 1, 2). This difference was mainly
related to the greater biomass of microplankton
123
94 Hydrobiologia (2013) 717:85–108

0,4
A) 0,3 B)
0,25
0,2
0,2
0 0,15
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs 0,1
-0,2 , 0,05 ,

0
-0,4 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
-0,05
-0,6 Bacteria ISCh -0,1 ANF ISCh
Bacteria MCh -0,15
ANF MCh
-0,8 -0,2
Mixed trophic impact index

0,3 C) 0,6 D)
0,2 0,4

0,1 0,2

0 , 0 ,
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs

-0,1 -0,2
Mphyto ISCh Cop.cal ISCh
-0,2 -0,4
Mphyto MCh Cop.cal MCh
-0,3 -0,6

0,6 E) 2 F)
0,5 1,5
0,4 1
0,3 0,5
0,2 0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
, -0,5 ,
0,1
-1
0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs -1,5
-0,1 -2 Scypho ISCh
-0,2 Euph ISCh
-2,5 Scypho MCh
-0,3 Euph MCh -3

Fig. 4 Mixed trophic impact index for the functional groups of belonging to ISCh and white bars to MCh. In A is presented
Inner Sea of Chiloe (ISCh) and Moraleda Channel (MCh). the MTI of Bacteria, B for ANF, C for Microphytoplankton,
Positive and negative impacts are represented by bars above and D Copepoda Calanoida, E Euphausiacea, F Scyphomedusae,
below the baseline, respectively. The height of the bars indicates G Siphonophora, H Clupeiformes adult-juvenile, I Gadiformes
relative impact, comparable among groups. The impacted adult, J Otariidae, K Aves, and L for Orcinus orca. The fisheries
functional groups are numbered as in Table 1. The impacting are, CFs = Clupeiformes Purse-seine; GFs = Gillnet fishery;
groups are named in each graph’s legend. Black bars indicate LFs = Long line fishery; MFs = Mackerel Purse-siene;
the mixed trophic impact index of the different species LhFs = Line hand fishery

(2.3 times more), bacteria (2.0), nanoflagellates (2.0), diatoms, autotrophic nanoflagellates, and bacteria
Copepoda (1.7), and secondarily to Carangidae (3.5), constituted 7.4, 0.9, and 3.4 % of the total biomass,
Ichthyoplankton (1.9), Clupeiformes (1.7), Sciaenidae unlike the MCh, where the percentages were lower
(100 %), and Atherinopsidae (1.7) observed in the (4.6, 0.8, and 2.6 %, respectively) (Table 1).
ISCh ecosystem (Table 1).
When we compare the biomasses of microphyto- Ecotrophic efficiency, energy flows, system
plankton, nanophytoplankton (ANF), and picoplank- throughput, and energy transfer efficiencies
ton (bacteria) in the ISCh and MCh, we obtained ratios
of 7.8:1.0:3.6 and 5.7:1.0:3.2, respectively. This Over 57 and 66 % of the functional groups had an
suggests a higher dominance of the microphytoplank- EE [ 0.9 in MCh and ISCh, respectively. Here,
ton (mainly diatoms) in the ISCh than in the MCh. In bacteria consumed only DOM and HNF consumed
addition, in the ISCh ecosystem, the biomasses of the only bacteria, whereas microflagellates were

123
Hydrobiologia (2013) 717:85–108 95

0,2 G) 1 H)
0,15 0,8
0,1
0,05 0,6
0 0,4
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
-0,05
, 0,2 ,
-0,1
-0,15 0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
-0,2 -0,2
-0,25 Sipho ISCh
-0,4 Clup (J-A) ISCh
-0,3 Sipho MCh
-0,35 -0,6 Clup (J-A) MCh

0,8 I) 0,2 J)
Mixed trophic impact index

0,1
0,6
0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
0,4 -0,1
0,2 -0,2
, -0,3 ,
0 -0,4
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs

-0,2 -0,5
-0,6 Otaria ISCh
-0,4 Gad (A) ISCh
-0,7 Otaria MCh
Gad (A) MCh
-0,6 -0,8

0,2 K) 0,6 L)
0,1 0,4
0 0,2
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
-0,1 0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs
-0,2 , -0,2 ,

-0,3 -0,4
-0,4 -0,6
Aves ISCh
-0,8
O.orca ISCh
-0,5 Aves MCh O.orca MCh
-0,6 -1

Fig. 4 continued

consumed by zooplankton, zooplankton by fishes, and and tertiary production) but only the PP was *3 times
these two latter groups were consumed by marine higher in MCh than ISCh (Table 2).
mammals, seabirds, fishes, and fisheries. Two groups The energy transfer efficiencies (ETE) of MCh and
of top predators had higher EEs: Aves, mainly due to ISCh were similar (32 vs. 30 %). However, the energy
cannibalistic behavior and fisheries interaction, and available from primary producers in ISCh (26 %) was
Delphinidae, due to predation and fisheries interaction slightly higher than in MCh (25 %). The relationship
(Table 1, Annex 3). between detritus (D) and biomass of primary produc-
The different biomasses found in the pelagic ers (PP), (D = DOM ? POC)/PP was 1.7 times
communities of these two ecosystems also produced higher in ISCh than MCh (i.e., MChD/PP = 35.8,
different carbon flows, consumption, exports, respira- ISChD/PP = 59.9). Moreover, the amount of energy
tion, and total system throughput (Table 2). For all available at the last trophic level was greater in ISCh
these parameters, ISCh showed from 1.7 to 1.9 times (9.3 %) than in MCh ecosystem (5.5 %).
more flows than MCh, e.g., total system throughput for
ISCh is 2.697 versus 1.432 gC m-2 year-1 for MCh Fisheries and fishing mortality rates
(Table 2). In the same way, all productions in the ISCh
were between 1.2 and 5.2 times higher than in MCh The total catch was ca. 20 times higher in ISCh than in
(i.e., net system production, all production, secondary, MCh (Table 2). Moreover in the ISCh ecosystem, only

123
96 Hydrobiologia (2013) 717:85–108

1
17 16 from that observed in MCh, where only one groups
0.5 had fishing mortality rates higher than predation
17 16
Keystone index

26 26
0
3 3
0 0.2
-0.5
-1
-1.5
-2
Fig. 5 Keystoneness for the functional groups of the pelagic
communities in the Inner Sea of Chiloe (ISCh) and Moraleda
Channel (MCh), sensu Libralato et al. (2006). For each
functional group, the keystoneness index (‘‘y’’ axis) is reported
against overall effect (‘‘x’’ axis). Overall effects are relative to
the maximum effect measured in each trophic web. Thus, for the
‘‘x’’ axis, the scale is between 0 and 1. The keystone functional
groups are those that have value close to or greater than zero, and
they are numbered in the graph. The functional groups are
numbered as in Table 1, where numbers in bold and cursive
correspond to ISCh and MCh, respectively
two functional groups have fishing mortality rates
higher than predation mortality rates (i.e., Otariidae by
incidental catch or bycatch, Gempylidae by direct
catch) (Table 3). However, when we compare fishing
with other natural mortalities (life history, senescence,
disease), fishing mortality exceeded 90 % of the
natural mortalities in eight groups (Aves and Delphin-
idae by incidental catch or bycatch, Scianidae, Gem-
pylidae, Atherinopsidae, Ophidiiformes, Gadiformes,
and Carangidae by direct catch; Table 3). In three of
these groups, mortalities from fishing activities com-
prise [30 % of total mortality. This situation differs
mortality rates (Otariidae by incidental catch or
0.4 0.6 0.8 1
15 bycatch), five groups had fishing mortality higher
15
than other natural mortalities (Delphinidae, Gempyli-
ISCh dae, Atherinopsidae, Ophidiiformes, Carangidae), and
MCh
one group had a fishing mortality [10 % of total
mortalities (Otariidae) (Table 3).
Relative total impact
The total catches of all fish resources were 194 and
10 mg C m-2 year-1 in ISCh and MCh, respectively,
and the most important species were Clupeiformes,
Carangidae, and Gadiformes in ISCh, and Gadiformes
and Clupeiformes species (caught by artisanal fisher-
ies) in MCh (Fig. 8). The bycatch levels for ISCh and
MCh were 0.7 and 0.3 mg C m-2 year-1, respec-
tively, with the most important species being Otariidae
and Aves (Fig. 7).
According to the mixed trophic impact analysis,
any increase in fisheries activities would affect both
commercial and non-commercial species (Fig. 8). In
these fisheries, greater Clupeiformes catches would
produce a negative effect, reducing Clupeiformes,
Gempylidae, and Otariidae biomasses and triggering
competition with Clupeiformes and hand-line fisheries
(Fig. 8A). Higher gillnet fisheries catches would
negatively affect the Otariidae and Delphinidae bio-
masses; the effect would be felt more strongly in ISCh
than MCh (Fig. 8B). Increased purse-seine catches of
mackerel would negatively affect Gempylidae and
Carangidae biomasses, producing competition with
hand-line and mackerel purse-seine fisheries

1000000.00000
100000.00000
Flows to detritus (mgC m-2 year -1)

10000.00000
1000.00000
100.00000
10.00000
1.00000
0.10000
0.01000
0.00100 ISCh (POC) MCh (POC)

0.00010 ISCh (DOM) MCh (DOM)

0.00001
1 2 3 4 5 6 7 8 9 10 12 13 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

Fig. 6 Carbon flow (mgC m-2 y-1) to detritus from the (ISCh). The functional groups are numbered as in Table 1. Note
different functional groups of the Northern Patagonia pelagic log scale in the abscise
system: Moraleda Channel (MCh) and Inner Sea of Chiloe

123
 Table 1 Data output on biomass (B), P/B ratio, Q/B ratio, P/Q ratio, EE for the different groups that represent the pelagic subweb of Inner Sea of Chiloé (ISCh) and Moraleda
Channel (MCh)
Trophic level Biomass (mgC/m2) Production/biomass Consumption/biomass Production/ Ecotrophic
(/year) (/year) Consumption efficiency
ISCh MCh ISCh MCh ISCh MCh ISCh MCh ISCh MCh ISCh MCh

1 Otariidae 5.91 5.54 22.19 17.27 0.09 0.09 6.32 6.15 0.014 0.014 0.211 0.179
2 Aves 5.23 5.14 15.33 11.27 0.10 0.10 7.29 7.29 0.014 0.014 0.994 0.860
3 Orcinus orca 5.76 5.60 0.01 0.18 0.06 0.06 11.58 11.58 0.005 0.005 0.000 0.000
Hydrobiologia (2013) 717:85–108

4 Mysticeti 4.51 4.49 0.29 3.07 0.04 0.04 10.10 9.32 0.004 0.005 0.083 0.154
5 Delphinidae 5.24 5.10 0.34 4.71 0.08 0.08 11.16 11.16 0.007 0.007 0.992 0.994
6 Gempylidae 5.32 5.17 11.00 11.41 0.09 0.09 0.47 0.47 0.198 0.198 0.991 0.995
7 Sciaenidae 5.20 – 359.76 – 0.11 – 0.40 – 0.269 – 0.998 –
8 Atherinopsidae 3.83 3.83 60.95 36.89 0.56 0.56 2.19 2.19 0.255 0.255 0.991 0.996
9 Ophidiiformes 5.09 5.02 266.62 204.11 0.11 0.11 0.53 0.53 0.212 0.212 0.995 0.993
10 Gadiformes (A) 4.65 4.56 1311.05 1829.35 0.12 0.12 0.44 0.43 0.265 0.275 0.991 0.694
11 Gadifomes (J-L) 4.39 3.91 353.85 528.59 0.28 0.31 0.74 0.73 0.381 0.433 0.975 0.997
12 Carangidae 4.65 4.63 588.43 168.53 0.09 0.09 0.42 0.42 0.218 0.218 0.993 0.995
13 Clupeiformes (J-A) 4.18 4.08 2466.22 1422.51 0.70 0.70 2.85 2.85 0.244 0.244 0.303 0.255
14 Clupeiformes (L) 3.83 3.83 146.44 86.72 1.65 1.73 7.73 7.77 0.214 0.222 0.992 0.991
15 Ichthyoplankton (L) 3.78 3.78 2071.69 1096.56 2.29 2.29 8.62 8.62 0.265 0.265 0.995 0.998
16 Scyphomedusae 4.26 4.26 85.28 53.68 41.06 41.06 116.25 113.88 0.353 0.361 0.008 0.019
17 Hydromedusae 3.91 3.90 23.75 34.06 32.24 32.24 101.42 101.42 0.318 0.318 0.659 0.311
18 Ctenophora 3.93 3.92 3.54 2.28 57.51 57.51 250.31 231.47 0.230 0.248 0.999 0.991
19 Appendicularia 2.50 2.50 9.25 6.61 158.51 158.51 523.49 523.49 0.303 0.303 0.999 0.996
20 Siphonophore 3.96 3.95 28.50 17.94 60.83 60.83 187.96 187.96 0.324 0.324 0.126 0.124
21 Salpida 3.41 3.41 3.62 3.85 39.35 39.35 131.12 131.12 0.300 0.300 0.998 0.996
22 Decapoda (L) 3.08 3.07 893.85 648.35 5.53 5.53 12.34 12.15 0.448 0.455 0.999 0.999
23 Euphausiacea 3.18 3.17 1556.64 949.38 5.37 5.37 17.58 17.58 0.305 0.305 0.997 0.997
24 Chaetognatha 3.72 3.72 17.76 11.76 11.73 11.73 50.76 50.76 0.231 0.231 0.997 0.997
25 Cladocera 3.36 3.36 4.47 2.92 52.40 52.40 149.58 149.58 0.350 0.350 0.999 0.991
26 Copepoda calanoida 2.64 2.63 1197.67 727.00 28.84 28.84 81.92 81.92 0.352 0.352 0.996 0.995
27 Copepoda cyclopoida 3.12 3.12 61.85 29.43 42.94 42.94 122.18 122.18 0.351 0.351 0.945 0.991
28 Copepoda nauplii (L) 3.04 3.04 33.36 86.63 46.03 46.03 131.37 131.37 0.350 0.350 0.995 0.321
29 Ciliophora 2.71 2.71 55.75 38.77 533.98 533.98 1167.20 1167.20 0.457 0.457 0.992 0.999
97

123
98 Hydrobiologia (2013) 717:85–108

0.180
0.995
0.389
0.837
0.914
0.886
0.009
(Fig. 8C). The long-line fishery would produce a

MCh
largely negative effect on the Otariidae, but positive in
Ecotrophic
efficiency
Scianidae, Ophidiiformes, Carangidae. Unfortunately,

0.165
0.887
0.268
0.683
0.933
0.996
0.009
ISCh
very little data was available on benthic-demersal
communities and, therefore, the real effect of long-line
0.457 fisheries was underestimated in this ecosystem by our
0.445

0.636
MCh

models, which focus on pelagic ecosystem (Fig. 8D).

Consumption

–
–
Production/

Increased hand-line fisheries catch would had negative

effect on Gempylidae group as well as on same fishery
0.457
0.445

0.636
ISCh

– activity by intraspecific effect (Fig. 8E).

–
1441.35
1597.53

1174.98

Discussion
Consumption/biomass

MCh

–
–

Similar to other ecosystem models that consider both

microbial and traditional food webs (Pavés & González,
2008), the application of EwE allowed us to charac-
1441.35
1597.53

1248.98
(/year)
ISCh

terize the trophic energy flows and amount of biomass

–

–
–

in the pelagic realm. In addition, with EwE it was

possible to determine the existence of a tight link
between the microbial loop and the traditional food
793.61
658.82
710.83
710.83
747.11
Production/biomass

MCh

web; a condition also mentioned in previous studies

–
–

(Sherr & Sherr, 1988; Pavés & González, 2008;

Reynolds, 2008).
541.24
658.82
710.83
710.83
794.57
(/year)
ISCh

Niche overlap index (TOI), prey and predator

–
–

overlap
24330.48
225.503

4055.08
403.30

In both ecosystems, the TOI values were highest for

27.56
93.66
70.85
Biomass (mgC/m2)

MCh

fish larvae and jellyfish; species become competitors

under conditions of limiting prey resources (i.e.,
34503.45

zooplankton). Swarms of either filter-feeding

5750.58
997.37

206.38
127.09
453.32

Bold numbers denote the data estimated by the EwE models

(0.6–5.0 salps l-1, Everett et al., 2011) or carnivorous

43.90
ISCh

jellyfishes (Purcell & Sturdevant, 2001; Arai, 2005)

are able to ‘‘clean’’ the water of potential food
MCh

particles reducing the food for other species (e.g.,

1.00
2.76
3.00
1.00
2.00
1.00
1.00
Trophic level

fishes). As similar salp abundances have been found in

the ISCh (Giesecke, unpublished data) negative effect
ISCh

were observed on the fishes, thus a strong competition

1.00
2.76
3.00
1.00
2.00
1.00
1.00

between fish larvae and jellyfishes cannot be ruled out.

Moreover, the jellyfish groups have higher P/B ratios
Microphytoplankton

(Palomares & Pauly, 2009; Table 1, Annex 1) and

fewer predators than fishes (Fig. 2), such that the
Microflagellates

former respond more quickly to environmental

Table 1 continued

changes with an accelerated rate of population growth.

Bacteria

Detritus
DOM

Thus, jellyfish could be more likely to benefit from the

HNF
ANF

competition (Arai, 2005). Jellyfish could also affect

the abundance of fish larvae and eggs (Purcell, 1981;
30
31
32
33
34
35
36

Larson, 1987; Carr & Pitt, 2008) and, thus, the

123
Hydrobiologia (2013) 717:85–108 99

Table 2 Summary of the

Parameter ISCh MCh Difference Unit
statistical data for Inner Sea
(times)
of Chiloe (ISCh) and
Moraleda Channel (MCh) Sum of all consumption 1225.92 633.02 1.9 gC m-2 year-1
for the pelagic sub-web off
the North Patagonian Sum of all exports 128.351 75.56 1.7 gC m-2 year-1
coastal ecosystem Sum of all respiratory flows 515.41 271.64 1.9 gC m-2 year-1
Sum of all flows into detritus 826.92 451.52 1.8 gC m-2 year-1
Total system throughput 2696.59 1431.74 1.9 gC m-2 year-1
Primary production 119.26 370.43 0.3 gC m-2 year-1
Bacteria production 360.19 168.48 2.1 gC m-2 year-1
Secondary and tertiary production 783.67 150.43 5.2 gC m-2 year-1
Sum of all production 1263.13 689.34 1.8 gC m-2 year-1
Net system production 114.75 98.79 1.2 gC m-2 year-1
Total biomass (excluding detritus) 13.48 8.85 1.5 gC m-2
Total catches 0.19 0.01 19 gC m-2 year-1

Table 3 Natural and fishing mortality rates on mainly artisanal fishing groups and discarded species in Inner Sea of Chiloe (ISCh,
bold values) and Moraleda Channel (MCh) for the pelagic sub-food web of the North Patagonian coastal ecosystem
Group name Ecosystem P/B or Z Fishing mort. ?Predation mort. ?Other mort. Fishing mort./ Proportion
(/year) rate (/year) rate (/year) rate (/year) total mort. natural mort.

Otariidae ISCh 0.088 0.018 0.000 0.069 0.209 0.791

MCh 0.088 0.011 0.005 0.072 0.125 0.875
Aves ISCh 0.099 0.018 0.080 0.001 0.184 0.816
MCh 0.099 0.005 0.080 0.014 0.050 0.950
Delphinidae ISCh 0.083 0.026 0.056 0.001 0.317 0.683
MCh 0.083 0.004 0.079 0.000 0.046 0.954
Gempylidae ISCh 0.092 0.068 0.023 0.001 0.741 0.259
MCh 0.092 0.002 0.090 0.000 0.018 0.982
Sciaenidae ISCh 0.107 0.002 0.105 0.000 0.020 0.980
MCh – – – – – –
Atherinopsidae ISCh 0.558 0.030 0.523 0.005 0.054 0.946
MCh 0.558 0.014 0.542 0.002 0.025 0.975
Ophidiiformes ISCh 0.112 0.006 0.105 0.001 0.055 0.945
MCh 0.112 0.002 0.109 0.001 0.020 0.980
Gadiformes (A) ISCh 0.117 0.008 0.108 0.001 0.068 0.932
MCh 0.117 0.004 0.077 0.036 0.036 0.964
Carangidae ISCh 0.092 0.035 0.057 0.001 0.376 0.624
MCh 0.092 0.001 0.090 0.000 0.012 0.988
Clupeiformes (A) ISCh 0.695 0.064 0.147 0.484 0.092 0.908
MCh 0.695 0.001 0.176 0.518 0.001 0.999

recruitment of fish populations (Lynam et al., 2005). producing negative effects over the whole trophic web
These situations have been observed during overfish- (Cury & Shannon, 2004; Arai, 2005; Frank et al.,
ing and strong eutrophication events, when the 2005; Daskalov et al., 2007). For example, in the
fisheries decreased dramatically or collapsed, in turn, Black sea, the overfishing of marine mammals and

123
100
Fig. 7 Catches of artisanal fishing resources (catch) and
incidental catches (bycatch) of marine mammals and seabirds
in the Inner Sea of Chiloe (ISCh) and Moraleda Channel (MCh)
small pelagic fishes has made the system more
vulnerable to jellyfish proliferation, resulting in a less
diverse and low-fish biomass system (Daskalov et al.,
2007). In the North Benguela Current System, the
trophic structure has shifted, due to overfishing, to a
system dominated by medusae, small pelagic gobiids,
mesopelagic fish, and horse mackerel (Cury & Shannon,
2004; Moloney, 2010).
Mixed trophic impact analysis
At the bottom of the food web built, the finding that
bacteria have a very strong intra-functional group effect
that would regulate their biomass and avoid fast and
sustained growth might help understand the stable size
observed in the different marine systems. Also, this effect
might be caused by multiple factors not assessed in this
model (e.g., chemical signals, DOM quality, bacteria cell
size) that could regulate both inter- and intraspecific
competition (Keller & Surette, 2006; Baquero & Lem-
onnier, 2009). Thus, in addition to these intra-group
regulation processes, several external factors that
enhance bacterial mortality (e.g., viral attack, bacteriv-
orous nanoflagellates) or growth rate mechanisms (low
requirements, efficient resource uptake) seem to be
comparable in magnitude, resulting in low bacterial
biomass variability (González et al., 2011).
The stronger effect of microphytoplankton than
ANF on the food web (by 2–4 times stronger) estimated
123
Hydrobiologia (2013) 717:85–108
here has been reported also in other studies (Iriarte &
González, 2004; González et al., 2010, 2011). These
authors have determined that picoplankton dominate in
periods of low productivity (winter) and El Niño
events, whereas microphytoplankton are predominant
during productive periods (spring) or La Niña events,
linking large-sized phytoplankton ([20 lm) with
higher levels of biomass in the pelagic systems (Iriarte
& González, 2004), similar to that described for
equatorial marine systems (Peña et al., 1990).
Moreover, the higher impact of Euphausiacea than
Copepoda calanoida on higher trophic levels exceeds
(by 4 and up to 150 times) the impact estimated here,
suggesting a more important role of Euphausiacea on
ecosystem productivity and energy flows, as expected
considering that krill are reported to be the preferred
food item of several fish species along the Humboldt
Current System (HCS) (Antezana, 2010). Such rela-
tions have been observed in several disparate systems
along the Chilean coast, including upwelling areas
along the HCS where they have been reported as key
species in the top–down control on primary producers,
carbon fluxes to the sediment, and principal prey for
upper trophic level such as fishes (González et al.,
2009; Antezana, 2010). In addition euphausiids seems
to be a keystone component in the transfer of
phytoplankton (and small-size plankton in general)
to a wide variety of top consumers in several
environments such as Patagonian fjords (Sánchez
et al., 2011) and Antarctic Ecosystem (Cornejo-
Donoso & Antezana, 2008).
The mixed trophic impact analyses permitted us
determinate that the Clupeiformes and Gadiformes
had a positive impact on higher trophic level and the
fisheries, but the intraspecific control-effect in Gadi-
formes is twofold higher than in Clupeiformes. This
situation could be related with the different cannibal-
ism level in these specie: where up to 60 % of the
Gadiformes diet was reported to be juveniles of the
same species (Lillo et al. 2005; Córdova et al. 2006;
Saavedra et al. 2007), and in contrast, Clupeiformes
prey on larval fish but apparently not on juveniles
(Espinoza & Bertrand, 2008; Prokopchuk, 2009).
Similar to Clupeiformes and Gadiformes, the top
predators (e.g., Aves, Otariidae, and O. orca) all
would have an important intra-functional group effect
that may determine their population trend and avoids
uncontrolled population growth. Within this top
predator group, several cases indicate that reinforced
Hydrobiologia (2013) 717:85–108 101

Fig. 8 Mixed trophic A) 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs

impact (MTI) index for the 0,1 0,002
different fisheries groups of
0,05 0,001
the Inner Sea of Chiloe
(ISCh) and Moraleda 0 0
Channel (MCh). Positive
and negative impacts are -0,05 , -0,001
represented by dots (black
-0,1 -0,002
and white) above and below
the baseline, respectively. Clupeiformes Purse-seine fishery ISCh
-0,15 -0,003
The height of the lines Clupeiformes Purse-seine fishery MCh
indicates relative impact, -0,2 -0,004
comparable among groups.
In A is presented the MTI of
B) 0,6 0,23
0,18
Clupeiformes Purse-seine, 0,4
0,13
B for Gillnet fishery, C for
Mackerel Purse-seine, 0,2 0,08
D Long line fishery, and 0,03
Mixed trophic impact index (ISCh)

0 ,

Mixed trophic impact index (MCh)

E for Line hand fishery. -0,02
Functional groups are -0,2 -0,07
numbered as in Table 1 Gillnet fishery ISCh
-0,12
-0,4 Gillnet fishery MCh
-0,17
-0,6 -0,22

C) 0,05 0,002
0 0
-0,05 -0,002
-0,1 -0,004
-0,15 -0,006
,
-0,2 -0,008
-0,25 -0,01
Mackerel Purse-seine fishery ISCh -0,012
-0,3
Mackerel Purse-seine fishery MCh
-0,35 -0,014
-0,4 -0,016

D) 0,3 0,6

0,2 0,4

0,1 0,2

0 , 0

-0,1 -0,2
Long line fishery ISCh
-0,2 Long line fishery MCh -0,4

-0,3 -0,6

E) 0,02 0,00018

0 -0,00002
-0,02
-0,00022
-0,04
-0,00042
-0,06 ,

-0,00062
-0,08
Line hand fishery ISCh
-0,1 -0,00082
Line hand fishery MCh
-0,12 -0,00102
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 CFs LFs LhFs

123
102
intraspecific competition and overfishing likely con-
tribute to a strong dietary shift (e.g., Southern sea
lion—Otaria flavescens, Drago et al., 2009), or
impacting the seabird community structure (Ballance
et al., 1997). In addition, the effects of intraspecific
competition in these top predators resulted in different
levels of aggressive behavior displayed under condi-
tions of limited resources or high population density
(e.g., sea lions and fur seals, Cassini, 2000; dolphins,
Samuels and Gifford, 1997; odontocete cetaceans,
MacLeod, 1998; baleen whales, Baker & Herman,
1984).
Moreover, we found more differences than simi-
larities in the effect that each functional group would
produce in these two modelled pelagic ecosystems.
Only bacteria would have the same effect in both
ecosystems through the whole food web. In this case,
even though the bacteria biomass was twice as higher
in the ISCh than MCh, its effect was the same, and,
therefore its role (function) would not change in these
environments. Different situation was registered in the
other groups, where the effect of each one of them was
different according to the preys, predators, and for
fisheries. All these differences and/or similarities of
the predators and preys trophic impact index, may
change dramatically depending on the specific char-
acteristics of the ecosystem under observation, and
thus will be a mistake to generalize the role of these
functional groups in the different environment.
Keystoneness of functional groups
In the ISCh and MCh ecosystems, the same groups
showed the highest keystoneness indexes (jellyfish,
copepods, Orca, fish larvae). This situation implies
that any change in the abundance of these groups,
especially the jellyfish (which have the highest
keystoneness value), could result in strong modifica-
tions of the ecosystem structure and functioning.
Similar situations have been observed in the South
Chilean fjords, where an increment in the jellyfish
abundance produced strong mortalities in salmon
farms (Giesecke, pers. comm., 2010) as well as in
other fish species (Cury & Shannon, 2004; Arai, 2005;
Frank et al., 2005; Daskalov et al., 2007). Moreover,
this situation had been observed in some ecosystem
models, particularly in 3 out of 16 ecosystem models
analyzed by Pauly et al. (2009) and covering different
habitats (from semi-enclosed waters to large areas of
123
Hydrobiologia (2013) 717:85–108
the open ocean) and levels of exploitation (from
heavily fished to targeting mainly top predators). In
our study, the smallest semi-enclosed ecosystem
shows the highest jellyfish keystoneness, similar to
the modeled results in past studies (i.e., Lancaster
Sound, Chesapeake Bay; Pauly et al., 2009).
Flow to the detritus and biomass
With this ecosystem approach it was possible to
highlight the importance of the microbial loop over
traditional food web for DOM and POC production.
Thus, the microbial loop produced 13 and 30 times
more POC than zooplankton and nekton groups (fish,
top predators) respectively, and 24 and 96-thousand
times more DOM than these groups. This suggests that
the microbial loop could be the key ecosystem
component to the functioning of the biological carbon
pump (Fig. 6). For other hand, the huge amount of
detritus matter that is produced but not consumed by
the high trophic levels, could exit these ecosystems as
material/energy input for demersal, coastal, or oceanic
ecosystems, typically as marine-snow resources that
are utilized by other species, (e.g., the mesopelagic
community, Wilson et al., 2008; migrating plankton,
Lampitt et al., 1993) or simply by organic matter
sinking to the sediment through the biological pump
(De La Rocha & Passow, 2007; Honjo et al., 2008;
González et al., 2009). This major contribution to the
detritus flows by the microbial loop could be related
with the higher P/B they have and, therefore, more
somatic production than the other functional group in
these models (Table 1). Moreover, in the ISCh it
produces 46 % more detritus than MCh, difference,
which is associated to the P/B ration and biomass of
each functional group in both ecosystems. However,
the biomass, because the P/B is very similar between
the models, would be the more important responsible
of this difference. In all groups and in the whole
ecosystem the biomass in ISCh is almost double than
MCh, for example, the microbial loop at the ISCh had
two times more biomass and more production than the
MCh (Fig. 6; Table 1). The double amount of biomass
in the ISCh than in the MCh could be related with the
fact that in the ISCh the phytoplankton was dominated
by microphytoplankton while in the MCh predomi-
nated nano- and picophytoplankton. At the ISCh we
found a micro- to nano-phytoplankton ratio[1, where
the microphytoplankton group represent more than
Hydrobiologia (2013) 717:85–108
7 % of the total biomass in the ecosystem, a fraction
that is 2.8 % higher than in MCh (Table 1).
Ecotrophic efficiency, energy flows, system
throughput, and energy transfer efficiencies
More than 50 % of the functional groups have an
EE [0.9 in the ecosystems compared, and 19 of them
had a similar value in both ecosystems (see Table 1),
and other 4, have a high EE value either in ISCh (Aves,
DOM) or in MCh (Microflagellates). These aspects
that show us differences in the functioning in the
ecosystems might be related mainly with the biomass
value of each functional group and the consumption
rate of their predator, because this is the only one
parameter with difference between ISCh and MCh.
In addition, the great amount of the functional
groups with EE [ 0.9 means that all production and
biomass is widely used in both ecosystems and,
therefore, these ecosystems would have a little surplus
production. We must, however, also consider the
existence of other groups, not considered herein due to
a lack of information, that might generate additional
impacts on these species (e.g., other species of fish,
crustaceans, cephalopods, Chondrichthyes, etc.).
Overall, the ecosystem production was utilized almost
totally and the incorporation of a new agent in these
ecosystems would imply that another existing group is
concerned, their biomass decreased or removed (if it is
a weak competitor), changing the ecosystem equilib-
rium state (Cury & Shannon, 2004; Arai, 2005; Frank
et al., 2005; Daskalov et al., 2007).
The different biomasses found in the pelagic
communities of these two ecosystems also produce
different carbon flows, consumption, exports, respira-
tion, total system throughput, and production. These
parameters were about two times higher in ISCh than
MCh. For example, the difference in productivity of
any high trophic level between these ecosystems
should be related to differences in the productivity of
the lower trophic levels (phytoplankton and zooplank-
ton) and may help explain the greater differences in
potential fisheries productivity of these ecosystems,
where the total catch is ca. 20 times higher in ISCh
than in MCh. This situation is probably related to the
type and amount of biological resources available in
the environments, which results from multivariate
parameters and conditions such as topographic char-
acteristics (Palma & Silva, 2004; Pavés et al.,
103
submitted), physical–chemical water characteristics
(Palma & Silva, 2004; Iriarte et al., 2007), marine
productivity (Iriarte et al., 2007), life histories of marine
fauna (nursery site, Bustos et al., 2007, 2008, 2011), and
marine biodiversity (Cassis et al., 2002; Hucke-Gaete
et al., 2004; Palma & Silva, 2004; Häussermann, 2006;
Reyes-Arriagada et al., 2007; Pavés & Schlatter,
2008; Zamorano-Abramson et al., 2010) within each
basin.
In relation to the energy transfer efficiencies (ETE)
the value in MCh and ISCh were similar (32 vs. 30 %),
and relatively high, probably because others models
did not include the microbial loop due to the shadow
effect produced by microbial species (see Christensen
et al., 2008). Our results show that an important part of
the energy flows through the bacteria group, which had
an ETE between 52 and 54 %, thus, increasing the
average ecosystem ETE up to levels of 32 %, how-
ever, the origin of this energy is from different sources.
The high ETE in MCh comes from detritus, whereas in
ISCh, this comes from primary producers. This
difference could also explain the greater amount of
energy available for the top trophic level of the ISCh
(9.3 %) vrsus the MCh ecosystem (5.5 %). This
relatively low level of energy in MCh could be due
to the relationship between the quantity and quality of
the food resources consumed. Thus, consumers that
feed mainly in ecosystems with a high quantity but low
quality of resources (i.e., MCh is rich in carbon-
dominated detritus) obtain less energy than consumers
that obtain energy from phytoplankton (i.e., ISCh is
rich in high quality phosphorus-dominated detritus).
This relation has also been observed in other ecosys-
tems (e.g., lakes: Hessen, 2008; Müller-Solger et al.,
2002, estuaries: Heinle et al., 1977), ingestion rate
experiments (Paffenhofer et al., 1995; Mayzaud et al.,
1998), and plankton food web models (Perhar &
Arhonditsis, 2009). All these approaches showed that
the highest zooplankton growth rates and egg produc-
tions were obtained in conditions where the diets are
based on natural assemblages of phytoplankton (live
food) rather than on a mixture of detritus (POC). In
addition, this should have implications for a more
efficient energy transfer to higher trophic levels.
Fisheries and fishing mortality rates
In the ISCh and MCh ecosystems, nine different
functional groups have fishing mortality rates higher
123
104
than the predation mortality rates (see Table 3).
Moreover, all functional groups under fisheries effect
(by catch ? capture) present higher mortalities in the
ISCh than the MCh ecosystems. Thus, in these
ecosystems under analysis, the levels of fisheries
pressure result in different effect on the fish resources.
This effect depends both on the biomass of each
functional group under direct or indirect (by-catches)
catches, as well as on the fishing effort of each fishery
in any of the specific ecosystems.
The ecosystem view allows us to determine that
fisheries activities affect both commercially important
and unimportant resources, the latter through bycatch,
with the non-commercial resources flowing directly to
the detritus. Thus, according to the mixed trophic
impact analysis, an increase in fisheries activities
would affect both commercial and non-commercial
species, as well as other fisheries activities. The
fisheries activities that produce more negative effect
on the catches of other fisheries are the Clupeiformes
(affect three fisheries), and mackerel fisheries (affect
two fisheries). However, this effect is 10–20 fold
higher between the fisheries activities in the ISCh
compared to the MCh ecosystem. These negative
effects on the marine biota and on the other fisheries
activities could be related to the un-selective catch of
the purse-seine fisheries (Clupeiformes, Carangidae),
as well as to the difference in the landing volumes
registered in these two ecosystems (see Annex 3).
Also, the mixed impact trophic data suggests that some
increase in the long line fisheries effort could affect
mainly the ISCh ecosystem, while the MCh ecosystem
could be more affected by a catch effort increase in the
purse-seine fisheries and gillnet fisheries.
Given the situation described for both pelagic
marine communities at both study areas, an increase
in the fishing effort—considering the high EE and
keystoneness of all fish groups, the seabird and marine
mammal by-catches, the cascade effects on commer-
cial resources and other species, and intraspecific
competition—could generate strong alterations in
these ecosystems, such as the decline of fisheries
resources and/or an increase of the gelatinous zoo-
plankton group. This shift has been reported frequently
and in disparate environments showing us the need to
increase our understanding of the marine system at the
ecosystem level, in order to develop an adequate
management policy on our marine resources at the
same time to enhance the ecosystem sustainability.
123
Hydrobiologia (2013) 717:85–108
Conclusions
Overall, the functioning of the two ecosystems studied
here showed that the energy that flows from detritus to
top predators is channeled through the same functional
groups. Some ecosystem parameters such as total
biomass flowing to detritus, fisheries catches, ETE
(from primary producers), secondary, and tertiary
production were twice as high in the basin with the
greater connection to the oceanic water and more
macronutrients supply (ISCh) than in the channel and
fjord area, which is protected from the oceanic water
effect and with has lower nutrient supply (MCh). Two
major lines of evidence seem to explain these
differences:
1. The size spectrum of plankton biomass: The
higher importance of microphytoplankton and
euphausiids at the ISCh, compared with nanofla-
gellates and copepods at the MCh, suggest that
larger preys may generate a more effective effect
in the trophic transfer toward top predators. Thus,
the higher zooplankton, fish biomass, top preda-
tor, and catches in ISCh compared to MCh may be
partially a consequence of the larger size of the
phyto- and zoo-plankton, than the PP per se.
2. The quality of the food resources consumed in the
lower trophic level: Consumers in systems dom-
inated by nitrogen and phosphorous-rich phyto-
plankton obtain more energy than the consumers
that feed mainly in ecosystems with a high
quantity but low quality of carbon-dominated
detritus. This affects the energy available from
one to the next trophic level. Again, the PP per se
seems not to be adequate proxy for predicting the
amount of secondary and tertiary production (up
to the fisheries level) in coastal marine systems.
Herein, we presented a general idea of the behavior
and trophic status of the two systems assayed. This
understanding could be improved through access to
more data generated by oceanographic surveys, stock
assessments, dietary ecology, and evaluations of by-
catch, amongst others. These models represent a first
step in helping us understand the structure and
functioning of the pelagic Patagonian ecosystems,
and to establish how fisheries activities affect them. A
strong local research line on autoecology, population
dynamics, and community studies should be encour-
aged in all taxa, as this would allow the generation of
Hydrobiologia (2013) 717:85–108
more local models. This, in turn can lead to the design
of appropriate management policies for natural
resources from an ecosystem approach—an initiative
which has not previously been attempted for Patago-
nian marine ecosystems.
Acknowledgments We thank our many colleagues who
provided the data, information, and constructive input that
allowed us to construct the trophic models for the southern
coastal system of Chile: Dr. Leonardo Castro and Maria Ines
Muñoz (Universidad de Concepción); Dr. Giovanni Daneri
(CIEP); and Dr. Edwin Niklisheck, Dr. Ricardo Giesecke,
Cecilia Torres (M.S.), Eduardo Menschel, Nicolás Sánchez, and
Marı́a José Calderón (Universidad Austral de Chile). The authors
thank the suggestions and comments of two anonymous reviewers
that substantially improved the original version of the MS. The
authors are indebted to all persons who have been working on the
development of the Ecopath approach since the early 1980s,
especially Carl Walters from Fisheries Centre (University of
British Columbia, Vancouver, Canada). Principal author (HP)
acknowledges the assistance provided by Jeroen Steenbeek,
Shawn Booth, and Andrés Cisneros during his postdoctorate
research at the Fisheries Centre (UBC). This study was funded by
the CIMAR-Fjords Program (grants 9, 12, and 13); FONDAP-
COPAS No. 15010007 Etapa II; Programa Financiamiento Basal
PFB-31/2007; and FONDECYT No. 1080187, and by the office of
Research and Development (Universidad Austral de Chile) (DID-
S-2010-45). HJP was supported by BECASCHILE Postdoctorate
Program 2010, the Fisheries Centre of University of British
Columbia, Vancouver, Canada, and the Postdoctorate Program
2011—Fondecyt No. 3120100 during the conduction of this
research. VC acknowledges support from the Nippon
Foundation—UBC Nereus Program and NSERC.
References
Allen, K. R., 1971. Relation between production and biomass.
Journal of the Fisheries Research Board of Canada 28:
1573–1581
Antacli, J., D. Hernández & M. Sabatini, 2010. Estimating
copepods’ abundance with paired nets: implications of
mesh size for population studies. Journal of Sea Research
63: 71–77.
Arcos, D., L. Cubillos & S. Núñez, 2001. The jack mackerel
fishery and El Niño 1997–98 effects off Chile. Progress in
Oceanography 49: 597–617.
Arcos, D., L. Cubillos & S. Núñez, 2004. Efectos de El Niño
1997–1998 sobre las principales pesquerı́as pelágicas de la
zona centro-sur de Chile. En: S. Avaria, J. Carrasco, J.
Rutllant, y E. Yáñez (eds) El Niño-La Niña 1997–2000.
Sus Efectos en Chile. CONA, Valparaı́so, Chile.
Antezana, T., 2010. Euphausia mucronata: A Keystone Herbi-
vore and Prey of the Humboldt Current System. Deep-Sea
Research Part II: Topical Studies in Oceanography 57:
652–662.
Arai, M. N., 2005. Predation on pelagic coelenterates: a review.
Journal of the Marine Biological Association of the United
Kingdom 85: 523–536.
105
Baker, C. S. & L. M. Herman, 1984. Aggressive behavior
between humpback whales (Megaptera novaeangliae)
wintering in Hawaiian waters. Canadian Journal of Zool-
ogy 62: 1922–1937.
Ballance, L. T., R. L. Pitman & S. B. Reilly, 1997. Seabird
community structure along a productivity gradient:
importance of competition and energetic constraint. Ecol-
ogy 78: 1502–1518.
Baquero, F. & M. Lemonnier, 2009. Generational coexistence
and ancestor’s inhibition in bacterial populations. FEMS
Microbiology Reviews 33: 958–967.
Bustos, C. A., F. Balbontı́n & M. F. Landaeta, 2007. Spawning
of the southern hake Merluccius australis (Pisces: Mer-
lucciidae) in Chilean fjords. Fisheries Research 83: 23–32.
Bustos, C. A., M. F. Landaeta & F. Balbontı́n, 2008. Spawning
and early nursery areas of anchoveta Engraulis ringens
Jenyns, 1842 in fjords of southern Chile. Revista de Bio-
logı́a Marina y Oceanografı́a 43: 381–389.
Bustos, C. A., M. F. Landaeta & F. Balbontı́n, 2011.
Ichthyoplankton spatial distribution and its relation with
water column stratification in fjords of southern Chile
(46°480 –50°090 S) in austral spring 1996 and 2008. Conti-
nental Shelf Research 31: 293–303.
Carr, E. F. & K. A. Pitt, 2008. Behavioural responses of zoo-
plankton to the presence of predatory jellyfish. Journal
of Experimental Marine Biology and Ecology 354:
101–110.
Cassini, M. H., 2000. A model on female breeding dispersion
and the reproductive systems of pinnipeds. Behavioural
Processes 51: 93–99.
Cassis, D., P. Muñoz & S. Avaria, 2002. Variación temporal del
fitoplancton entre 1993 y 1998 en una estación fija del seno
Aysén, Chile (45o260 S 73o000 W). Revista de Biologı́a
Marina y Oceanografı́a 37: 43–65.
Christensen, V., 1995. Ecosystem maturity: towards quantifi-
cation. Ecological Modelling 77: 3–32.
Christensen, V. & D. Pauly, 1992. ECOPATH II: a software for
balancing steady-state ecosystem models and calculating
network characteristics. Ecological Modelling 61:
169–185.
Christensen, V., C., Walters &, D. Pauly, 2000. Ecopath with
Ecosim: A User0 s Guide, October 2000. Fisheries Centre,
University of British Columbia, Vancouver, Canada and
ICLARM, Penang, Malaysia.
Christensen, V. & C. Walters, 2004. Ecopath with Ecosim:
methods, capabilities and limitations. Ecological Model-
ling 172: 109–139.
Christensen, V. & C. J. Walters, 2011. Progress in the use of
ecosystem modeling for fisheries management. In Chris-
tensen, V. & J. L. Maclean (eds), Ecosystem Approaches to
Fisheries: A Global Perspective. Cambridge University
Press, Cambridge: 189–205.
Christensen, V., C. Walters, D. Pauly, R. Forrest, 2008. Ecopath
with Ecosim version 6: A User0 s Guide, October 2008.
Fisheries Centre, University of British Columbia, Van-
couver, Canada and Lenfest Ocean Futures Project, Van-
couver, Canada.
Córdova, J., R. Céspedes, V. Ojeda, F. Balbontı́n, P. Rojas, A.
Saavedra, M. A. Barbieri & J. C. Saavedra, 2006. Evalu-
ación del stock desovante de merluza del sur y merluza de
cola en la zona sur austral, año 2005 (2da. Licitación).
123
106
Informe Final Fondo de Investigación Pesquera. FIP
2005-04. Valparaı́so, Chile. http://www.fip.cl.
Cornejo-Donoso, J. & T. Antezana, 2008. Preliminary trophic
model of the Antarctic Peninsula Ecosystem (Sub-area
CCAMLR 48.1). Ecological Modelling 218: 1–17.
Cury, P. & L. Shannon, 2004. Regime shifts in upwelling eco-
systems: observed changes and possible mechanisms in the
northern and southern Benguela. Progress in Oceanogra-
phy 60: 223–243.
Davila, P., D. Figueroa & E. Muller, 2002. Freshwater input into
the coastal ocean and its relation with the salinity distri-
bution off austral Chile (35–55°S). Continental Shelf
Research 22: 521–534.
Daskalov, G. M., A. N. Grishin, S. Rodionov & V. Mihneva,
2007. Trophic cascades triggered by overfishing reveal
possible mechanisms of ecosystem regime shifts. Pro-
ceedings of the National Academy of Sciences of the
United States of America 104: 10518–10523.
De La Rocha, C. L. & U. Passow, 2007. Factors influencing the
sinking of POC and the efficiency of the biological carbon
pump. Deep-Sea Research Part II: Topical Studies in
Oceanography 54: 639–658.
Drago, M., E. A. Crespo, A. Aguilar, L. Cardona, N. Garca, S.
L. Dans & N. Goodall, 2009. Historic diet change of the
South American sea lion in Patagonia as revealed by iso-
topic analysis. Marine Ecology Progress Series 384:
273–286.
Escribano, R., G. Daneri, L. Farı́as, V. A. Gallardo, H. E. Gon-
zález, D. Gutierrez, C. B. Lange, et al., 2004. Biological
and chemical consequences of the 1997–1998 El Niño in
the Chilean coastal upwelling system: a synthesis. Deep
Sea Research II 51: 2389–2411.
Espinoza, P. & A. Bertrand, 2008. Revisiting Peruvian anchovy
(Engraulis ringens) trophodynamics provides a new vision
of the Humboldt Current system. Progress in Oceanogra-
phy 79: 215–227.
Everett J. D., M. E. Baird & I. M. Suthers, 2011. Three-
dimensional structure of a swarm of the salp Thalia de-
mocratica within a cold-core eddy off southeast Australia.
Journal of Gophysical Research 116: C12046. doi:
10.1029/2011JC007310.
Frank, K. T., B. Petrie, J. S. Choi & W. C. Leggett, 2005.
Trophic cascades in a formerly cod-dominated ecosystem.
Science 308: 1621–1623.
Gallienne, C. P. & D. B. Robins, 2001. Is Oithona the most
important copepod in the world’s oceans? Journal of
Plankton Research 23: 1421–1432.
Giesecke, R. & H. E. González, 2004. Feeding of Sagitta enflata
and vertical distribution of chaetognaths in relation to low
oxygen concentrations. Journal of Plankton Research 26:
475–486.
González, H. E., G. Daneri, J. L. Iriarte, B. Yannicelli, E.
Menschel, C. Barrı́a, S. Pantoja & L. Lizárraga, 2009.
Carbon fluxes within the epipelagic zone of the Humboldt
Current System off Chile: the significance of euphausiids
and diatoms as key functional groups for the biological
pump. Progress in Oceanography 83: 217–227.
González, H. E., M. J. Calderón, L. Castro, A. Clement, L.
A. Cuevas, G. Daneri, J. L. Iriarte, L. Lizrraga, R. Martnez,
E. Menschel, N. Silva, C. Carrasco, C. Valenzuela, C.
A. Vargas & C. Molinet, 2010. Primary production and
123
Hydrobiologia (2013) 717:85–108
plankton dynamics in the Reloncavı́ Fjord and the Interior
Sea of Chiloé, Northern Patagonia, Chile. Marine Ecology
Progress Series 402: 13–30.
González, H. E., L. Castro, G. Daneri, J. L. Iriarte, N. Silva, C.
A. Vargas, R. Giesecke & N. Sánchez, 2011. Seasonal
plankton variability in Chilean Patagonia fjords: carbon
flow through the pelagic food web of Aysen Fjord and
plankton dynamics in the Moraleda Channel basin. Con-
tinental Shelf Research 31: 225–243.
Häussermann, V., 2006. Biodiversity of Chilean sea anemones
(Cnidaria: Anthozoa): distribution patterns and zoogeo-
graphic implications, including new records for the fjord
region. Investigaciones Marinas 34: 23–35.
Heinle, D. R., R. P. Harris, J. F. Ustach & D. A. Flemer, 1977.
Detritus as food for estuarine copepods. Marine Biology
40: 341–353.
Hessen, D., 2008. Efficiency, energy and stoichiometry in
pelagic food webs; reciprocal roles of food quality and food
quantity. Freshwater Reviews 1: 43–57.
Honjo, S., S. J. Manganini, R. A. Krishfield & R. Francois, 2008.
Particulate organic carbon fluxes to the ocean interior and
factors controlling the biological pump: a synthesis of
global sediment trap programs since 1983. Progress in
Oceanography 76: 217–285.
Hucke-Gaete, R., L. P. Osman, C. A. Moreno, K. P. Findlay &
D. K. Ljungblad, 2004. Discovery of a blue whale feeding
and nursing ground in southern Chile. Proceedings of the
Royal Society B: Biological Science 271: 170–173.
Iriarte, J. L. & H. E. González, 2004. Phytoplankton size
structure during and after the 1997/98 El Niño in a coastal
upwelling area of the northern Humboldt Current System.
Marine Ecology Progress Series 269: 83–90.
Iriarte, J. L., H. E. González, K. K. Liu, C. Rivas & C. Valen-
zuela, 2007. Spatial and temporal variability of chlorophyll
and primary productivity in surface waters of southern
Chile (41.5–43°S). Estuarine, Coastal and Shelf Science
74: 471–480.
Keller, L. & M. G. Surette, 2006. Communication in bacteria: an
ecological and evolutionary perspective. Nature Reviews
Microbiology 4: 249–258.
Lampitt, R. S., K. F. Wishner, C. M. Turley & M. V. Angel,
1993. Marine snow studies in the Northeast Atlantic
Ocean: distribution, composition and role as a food source
for migrating plankton. Marine Biology 116: 689–702.
Larson, R. J., 1987. Daily ration and predation by medusae and
ctenophores in Saanich Inlet, B.C., Canada. Netherlands
Journal of Sea Research 21: 35–44.
Libralato, S., V. Christensen & D. Pauly, 2006. A method for
identifying keystone species in food web models. Eco-
logical Modelling 195: 153–171.
Lillo, S., R. Céspedes, V. Ojeda, F. Balbontı́n, R. Bravo, A.
Saavedra, M. A. Barbieri & C. Vera, 2005. Evaluación del
stock desovante de merluza del sur y merluza de cola en la
zona sur austral, año 2004. Informe Final Fondo de In-
vestigación Pesquera. FIP 2004-07. Valparaı́so, Chile.
http://www.fip.cl.
Lindeman, R. L., 1942. The trophic-dynamic aspect of ecology.
Ecology 23: 399–418.
Lynam, C. P., S. J. Hay & A. S. Brierley, 2005. Jellyfish
abundance and climatic variation: contrasting responses in
oceanographically distinct regions of the North Sea, and
Hydrobiologia (2013) 717:85–108
possible implications for fisheries. Journal of the Marine
Biological Association of the United Kingdom 85:
435–450.
MacLeod, C. D., 1998. Intraspecific scarring in odontocete
cetaceans: an indicator of male ‘‘quality’’ in aggressive
social interactions? Journal of Zoology 244: 71–77.
Mattern, T., U. Ellenberg, G. Luna-Jorquera & Ll. S. Davis,
2004. Humboldt Penguin Census on Isla Chañaral, Chile:
recent increase or past underestimate of penguin numbers?
Waterbirds 27: 368–376.
Mayzaud, P., V. Tirelli, J. M. Bernard & O. Roche-Mayzaud,
1998. The influence of food quality on the nutritional
acclimation of the copepod Acartia clausi. Journal of
Marine Systems 15: 483–493.
Moloney, C. L., 2010. The humble bearded goby is a keystone
species in Namibia’s marine ecosystem. South African
Journal of Science 106: 1–2.
Müller-Solger, A. B., A. D. Jassby & D. C. Müller-Navarra,
2002. Nutritional quality of food resources for zooplankton
(daphnia) in a tidal freshwater system (Sacramento-San
Joaquin River Delta). Limnology and Oceanography 47:
1468–1476.
Odum, E. P., 1969. The strategy of ecosystem development.
Science 104: 262–270.
Odum, E. & E. Heald, 1975. The detritus-based food web of an
estuarine mangrove community. In Cronin, L. E. (ed.),
Estuarine Research, Vol. 1. Academic Press, New York:
265–286.
Oliveira, L. R., M. Arias-Schreiber, D. Meyer & J. S. Morgante,
2006. Effective population size in a bottlenecked fur seal
population. Biological Conservation 131: 505–509.
Paffenhofer, G. A., M. H. Bundy, K. D. Lewis & C. Metz, 1995.
Rates of ingestion and their variability between individual
calanoid copepod: direct observations. Journal of Plankton
Research 17: 1573–1585.
Palma, S. & N. Silva, 2004. Distribution of siphonophores,
chaetognaths, euphausiids and oceanographic conditions in
the fjords and channels of southern Chile. Deep-Sea
Research Part II: Topical Studies in Oceanography 51:
513–535.
Palomares, M. L. D. & D. Pauly, 2009. The growth of jellyf-
ishes. Jellyfish blooms: causes, consequences, and recent
advances. Hydrobiologia 616: 11–21.
Pauly, D., V. Christensen & C. Walters, 2000. Ecopath, Ecosim,
and Ecospace as tools for evaluating ecosystem impact of
fisheries. ICES Journal of Marine Science 57: 697–706.
Pauly, D., W. Graham, S. Libralato, L. Morissette & M. L. Deng
Palomares, 2009. Jellyfish in ecosystems, online databases,
and ecosystem models. Hydrobiologia 616: 67–85.
Pavés, H. J. & R. P. Schlatter, 2008. Temporada reproductiva del
lobo fino austral, Arctocephalus australis (Zimmerman,
1783) en la Isla Guafo, Chiloé, Chile. Revista Chilena de
Historia Natural 81: 137–149.
Pavés, H. J. & H. E. González, 2008. Carbon fluxes within the
pelagic food web in the coastal area off Antofagasta (23°S),
Chile: the significance of the microbial versus classical
food webs. Ecological Modelling 212: 218–232.
Pavés, H. J., H. E. González & J. L. Iriarte (unpublished data).
Carbon flows through the pelagic sub-foodweb in two
basins of the Chilean Patagonian coastal system: the
107
significance of coastal-ocean connection on ecosystemic
parameters.
Peña, M. A., M. R. Lewis & W. G. Harrison, 1990. Primary
productivity and size structure of phytoplankton biomass
on a transect of the equator at 135°W in the Pacific Ocean.
Deep-Sea Research Part I: Oceanographic Research Papers
37: 295–315.
Perhar, G. & G. B. Arhonditsis, 2009. The effects of seston food
quality on planktonic food web patterns. Ecological
Modelling 220: 805–820.
Prokopchuk, I., 2009. Feeding of the Norwegian spring
spawning herring Clupea harengus (Linne) at the different
stages of its life cycle. Deep-Sea Research Part II: Topical
Studies in Oceanography 56: 2044–2053.
Purcell, J. E., 1981. Dietary composition and diel feeding pat-
terns of epipelagic siphonophores. Marine Biology 65:
83–90.
Purcell, J. E. & M. V. Sturdevant, 2001. Prey selection and
dietary overlap among zooplanktivorous jellyfish and
juvenile fishes in Prince William Sound, Alaska. Marine
Ecology: Progress Series 210: 67–83.
Reyes-Arriagada, R., P. Campos-Ellwanger, R. P. Schlatter & C.
Baduini, 2007. Sooty Shearwater (Puffinus griseus) on
Guafo Island: the largest seabird colony in the world?
Biodiversity and Conservation 16: 913–930.
Reynolds, C., 2008. A changing paradigm of pelagic food webs.
International Hydrographic Review 93: 517–531.
Riccardi, N., 2010. Selectivity of plankton nets over mesozoo-
plankton taxa: implications for abundance, biomass and
diversity estimation. Journal of Limnology 69: 287–296.
Saavedra, A., V. Correa, R. Céspedes, V. Ojeda, L. Adasme, E.
Dı́az, J. Oliva & P. Rojas, 2007. Evaluación hidroacústica
del stock parental de merluza de tres aletas en su unidad de
pesquerı́a, año 2005. Informe Final Corregido Fondo de
Investigación Pesquera. FIP 2005-06. Valparaı́so, Chile.
http://www.fip.cl.
Samuels, A. & T. Gifford, 1997. A quantitative assessment of
dominance relations among bottlenose dolphins. Marine
Mammal Science 13: 70–99.
Sánchez, N., H. E. González & J. L. Iriarte, 2011. Trophic
interactions of pelagic crustaceans in Comau Fjord (Chile):
their role in the food web structure. Journal of Plankton
Research 33: 1212–1229.
Silva, N. & S. Palma, 2008. Progress in the oceanographic
knowledge of Chilean Interior Waters, from Puerto Montt
to Cap Horn. Comité Oceanográfico Nacional—Pontificia
Universidad Católica de Valparaı́so, Valparaı́so, Chile.
Sherr, B. & E. Sherr, 1988. Role of microbes in pelagic food
webs: a revised concept. Limnology and Oceanography 33:
1225–1227.
Smith, R. C., K. S. Baker, H. M. Dierssen, S. E. Stammerjohn &
M. Vernet, 2001. Variability of primary production in an
Antarctic marine ecosystem as estimated using a multi-
scale sampling strategy. American Zoologist 41: 40–56.
Stehle, M., A. Dos Santos & H. Queiroga, 2007. Comparison of
zooplankton sampling performance of Longhurst–Hardy
Plankton Recorder and Bongo nets. Journal of Plankton
Research 29: 169–177.
Vargas, C. A. & L. P. Madin, 2004. Zooplankton feeding
ecology: clearance and ingestion rates of the salps Thalia
123
108
democratica, Cyclosalpa affinis and Salpa cylindrica on
naturally occurring particles in the Mid-Atlantic Bight.
Journal of Plankton Research 26: 827–833.
Walters, C., D. Pauly & V. Christensen, 1999. Ecospace: pre-
diction of mesoscale spatial patterns in trophic relation-
ships of exploited ecosystems, with emphasis on the
impacts of marine protected areas. Ecosystems 2: 539–554.
Wilson, S. E., D. K. Steinberg & K. O. Buesseler, 2008. Changes
in fecal pellet characteristics with depth as indicators of
123
Hydrobiologia (2013) 717:85–108
zooplankton repackaging of particles in the mesopelagic
zone of the subtropical and subarctic North Pacific Ocean.
Deep-Sea Research Part II-Topical Studies in Oceanogra-
phy 55: 1636–1647.
Zamorano-Abramson, J., J. Gibbons & J. Capella, 2010.
Diversity and summer distribution of cetaceans in inlet
waters of Northern Aisén, Chile. Anales Instituto Patagonia
(Chile) 38: 151–157.