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Reduction of ecosystem connectivity has long-lasting impacts on food webs. Anadromous fish, which migrate from marine to freshwater ecosystems to complete reproduction, have seen their historically larger ecosystem role undercut by widespread riverine habitat fragmentation and other impacts mainly derived from anthropogenic sources. The result has been extensive extirpations and increased susceptibility to a suite of environmental factors that currently impede recovery. Under this present-day context of reduced productivity and connectivity, aggressive management actions and enforcement of catch limits including bycatch caps and complete moratoria on harvest have followed. What remains less understood are the implications of changes to food webs that co-occurred. What benefits restoration could provide in terms of ecosystem functioning in relation to economic costs associated with dam removal and remediation is unknown and can limit the scope and value of restoration activities. Here we employ, historical landscape-based biomass estimates of anadromous alosine for the first time in an ecosystem modeling of the Northeast US large marine ecosystem (LME), to evaluate the value of improving connectivity by measuring the increase in energy flow and population productivity. We compared a restored alosine model to a contemporary model, analyzing the impacts of the potential increase of connectivity between riverine and oceanic systems. There was the potential for a moderate biomass increase of piscivorous species with high economic value, including Atlantic cod, and for a major increase for species of conservation concern such as pelagic sharks, seabirds and marine mammals. Our study highlights the benefits of increased connectivity between freshwater and ocean ecosystems. We demonstrate the significant role anadromous forage fish could play in improving specific fisheries and overall ecosystem functioning, mainly through the diversification of species capable of transferring primary production to upper trophic levels , adding to benefits associated with their restoration.plo
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Opening the tap: Increased riverine
connectivity strengthens marine food web
Beatriz S. DiasID
*, Michael G. Frisk
, Adrian Jordaan
1Environmental Conservation Department, University of Massachusetts Amherst, Amherst, Massachusetts,
United States of America, 2CAPES Foundation, Ministry of Education of Brazil, Brası
´lia-DF, Brazil, 3School of
Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, United States of America
Reduction of ecosystem connectivity has long-lasting impacts on food webs. Anadromous
fish, which migrate from marine to freshwater ecosystems to complete reproduction, have
seen their historically larger ecosystem role undercut by widespread riverine habitat frag-
mentation and other impacts mainly derived from anthropogenic sources. The result has
been extensive extirpations and increased susceptibility to a suite of environmental factors
that currently impede recovery. Under this present-day context of reduced productivity and
connectivity, aggressive management actions and enforcement of catch limits including
bycatch caps and complete moratoria on harvest have followed. What remains less
understood are the implications of changes to food webs that co-occurred. What benefits
restoration could provide in terms of ecosystem functioning in relation to economic costs
associated with dam removal and remediation is unknown and can limit the scope and value
of restoration activities. Here we employ, historical landscape-based biomass estimates of
anadromous alosine for the first time in an ecosystem modeling of the Northeast US large
marine ecosystem (LME), to evaluate the value of improving connectivity by measuring the
increase in energy flow and population productivity. We compared a restored alosine model
to a contemporary model, analyzing the impacts of the potential increase of connectivity
between riverine and oceanic systems. There was the potential for a moderate biomass
increase of piscivorous species with high economic value, including Atlantic cod, and for a
major increase for species of conservation concern such as pelagic sharks, seabirds and
marine mammals. Our study highlights the benefits of increased connectivity between fresh-
water and ocean ecosystems. We demonstrate the significant role anadromous forage fish
could play in improving specific fisheries and overall ecosystem functioning, mainly through
the diversification of species capable of transferring primary production to upper trophic lev-
els, adding to benefits associated with their restoration.
PLOS ONE | May 23, 2019 1 / 27
Citation: Dias BS, Frisk MG, Jordaan A (2019)
Opening the tap: Increased riverine connectivity
strengthens marine food web pathways. PLoS ONE
14(5): e0217008.
Editor: Brian R. MacKenzie, Technical University of
Denmark, DENMARK
Received: October 31, 2018
Accepted: May 2, 2019
Published: May 23, 2019
Copyright: ©2019 Dias et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript, Supporting Information
files, and from the Dryad data repository (doi:10.
Funding: CAPES supported BSD through a PhD
grant (99999.001096/2013-03). This research was
also funded by the Lenfest Ocean Program at Pew
Charitable Trusts (CID 00025472). The funders had
no role in study design, data collection and
analysis, decision to publish, or preparation of the
Small pelagic finfish, characterized by extraordinary, yet highly variable abundance, are vital
components of global food webs [1]. In the North Atlantic, these so-called forage fish make
long migrations along the continental shelf in large schools of conspecifics (e.g., Atlantic men-
haden [Brevoortia tyrannus], [2]) or among mixed species (e.g., Atlantic herring [Clupea har-
engus], mackerel [Scomber scombrus] and river herring [3]). They feed almost exclusively on
planktivorous organisms as juveniles, and most add small invertebrates and fishes to their
diets as adults. At all life stages, forage fish transfer primary production to higher trophic
levels as they are consumed by diverse marine predators, including bony fish, elasmobranchs,
marine mammals, and seabirds [4].
Ecosystem connectivity, the movement of energy, inert material, nutrients and organisms
across physical or biological system boundaries, enhances the function and health of aquatic
ecosystems [5,6]. Forage fish add substantially to ecosystem connectivity by translocating
nutrients along migratory highways in their seasonal processions from spawning grounds to
feeding grounds. Occupying distinct habitats as temporary inhabitants of coastal and marine
ecosystems, pulses of prey species enrich successive food bases along the way [7], simulta-
neously providing trophic and geographic connectivity, and supporting vital coastal and off-
shore fisheries.
Historical records and recent research correlate the seasonal occurrence of forage fish spe-
cies to the movements and habitat preferences of cod and other groundfish [8,9]. It should not
be surprising, then, that loss of forage species is associated with marine ecosystem decline.
Deficient quantity and quality of the forage base have been linked to apex predator’s poor
physical condition, low productivity, and the failure of population recovery after depletion
events [10,11]. Along with global warming, spatiotemporal mismatch with lipid-rich prey may
reduce even more the productivity in highly valuable fished populations, such as the Gulf of
Maine’s Atlantic cod stocks (Gadus morhua), exacerbating their decline, or impairing their
recovery [12]. The recent recovery of capelin (Mallotus villosus), a lipid-rich forage species,
spurred growth in Newfoundland’s cod stocks, depressed since the mid-1990s [13]. As warm-
ing waters continue to shift the spatial range and timing of fish migrations, mismatches caused
by reduced predator and prey overlap becomes more frequent [14].
Whereas questions remain about the importance of single predator-prey linkages in driving
productivity across larger ecosystems [15], complex life histories likely contribute consistency
to predator-prey relationships [16,17]. For instance, capelin have two spawning modes, both
of which contribute to stock productivity [18,19]. Forage species that spawn in freshwater or
brackish estuaries and marshes only enter the marine food web after their eggs and larvae
develop into juvenile fish, and thus they may play complementary, but different ecosystem
roles compared to marine spawners like Atlantic herring.
River herring, anadromous alosines including alewife (Alosa pseudoharengus) and blueback
herring (Alosa aestivalis), are coastal forage species that spend most of their lives at sea, where
schools of adults often merge with larger schools of mature Atlantic herring and mackerel
[3,20,21]. Every year, however, most return to fresh water to spawn in natal grounds [22].
Extreme abundance of these fish in the Northeast US Large Marine Ecosystem (LME) (Fig 1)
and their annual transition between fresh- and saltwater, ensured a strong flow of energy
between marine and upland ecosystems [23] and abundant forage for predators, particularly
where rivers join the sea. However, river herring stocks throughout the LME were depleted as
dams impeded or blocked upwards of 95% of freshwater spawning habitat compared to pre-
colonial conditions [23,24]. Linkages between marine and freshwater systems unraveled [25]
as these key prey species became functionally extinct throughout most of their range.
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 2 / 27
Competing interests: The authors have declared
that no competing interests exist.
Current interest in the status of alewives and the success of dam removal and improved fish
passage in increasing alewife abundance, particularly in Maine [26,27], encouraged us to test,
via ecosystem modeling, the impacts of increasing anadromous forage fish populations on
marine food webs. First, we estimated potential alewife production in three Maine watersheds
(Androscoggin, Kennebec, and Penobscot) based on the spawning habitat potentially available
to them. Then, we employed that estimate in an Ecopath with Ecosim model framework to
assess how significantly increasing forage might impact predators in the Northeast US (NEUS)
LME (Fig 1). We built two EwE models for comparison. The Contemporary Alosine Biomass
(CAB) model reflects actual ecosystem conditions in the year 2000 (Fig 2). The Restored Alo-
sine Biomass (RAB) model incorporates estimated alewife production on the three watersheds
before 1600, prior to dam construction (Fig 1). Because alewives spawn far inland and are
sensitive to river fragmentation and other environmental alterations [28], the RAB scenario
Fig 1. Map of the study area and sub-regions included in both models. This map shows the bathymetric profile of
the coastal region, and NEUS LME ecoregions: The Gulf of Maine (GOM), Georges Bank (GB), Southern New
England (SNE), and Middle Atlantic Bight (MAB). The limits of the tan region also represent the US Exclusive
Economic Zone (EEZ).
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 3 / 27
assumes that adult biomass scales linearly with access to spawning habitat. Specifically, the
objectives were: 1) to quantify estimates of biomass change for managed species targeted by
fisheries or are species of concern; 2) to quantify changes in biomass flows from middle to
upper trophic levels; 3) to provide context for the role of anadromous forage fish in the NEUS
LME, the historical loss, and the impacts of river restoration on marine ecosystems.
Rather than match the spatial extent of our models to the spatial scale of our historical
estimates (the Gulf of Maine), we chose instead to model the entire NEUS LME. The
approach conforms to modern stock assessment methods and management where popula-
tion assessments are generally conducted over the whole range of a species or stock (within
national boundaries). Alewife stocks extend from Labrador to North Carolina [29], and Gulf
of Maine populations are likely to occupy a broader region throughout the NEUS LME dur-
ing the three to four years of full marine occupancy. Restoration goals were established based
on data from the second half of the 20
century [30], as they were intended for other man-
aged marine species within the LME. Setting restoration targets to recent baselines neglect
both the historical productivity of individual species and the system productivity derived
from trophic integrity and connectivity and in this case a long history of habitat loss under-
mining these key aspects.
Evolution from single species to ecosystem-based management (EBM) requires under-
standing trophic interactions and anthropogenic disturbances across variable temporal and
spatial scales [31]. Here, we employ a novel deployment of EwE to explore the value of increas-
ing forage species abundance, including consequences on predators, improvements to envi-
ronmental health, delivery of ecosystem services, and human well-being.
Fig 2. Flow diagram of the Contemporary Alosine Biomass model. The color gradient represents the direction of flow;
different life stages are represented by small (S), medium (M) and Large (L). Functional groups are ordered by trophic level.
Grey bubbles represent all functional groups, the pink bubble in bold letters represents anadromous alosine, and orange
bubbles represent fishing fleets.
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 4 / 27
Materials and methods
Species of interest
To assess the impacts of a potential increase in forage fish biomass on the marine environment,
we focused on alewife (A.pseudoharengus). Alewife is the flagship species within the anadro-
mous alosine group for several reasons. Due to spawning habitat preferences, they are most
vulnerable to changes in river connectivity, but they are also good indicators of the health of
other anadromous species that spawn in rivers and the upper bounds of estuaries [23,32].
Moreover, they have the highest potential for population restoration among anadromous
species [33], and have been the most responsive to increases in spawning habitat after dam
removal. Unlike menhaden or Atlantic herring, which support managed fisheries and are con-
sidered to be at adequate population levels, alewife is a candidate for protection under the US
Endangered Species Act [34], and catching the fish is banned throughout much of their US
range, except for the State of Maine. Concerted state and federal efforts are underway to
restore access to spawning habitat along alewife’s range, including the three major watersheds
considered here.
Our study is based on previous work by Hall et al. [28] and Mattocks et al. [23], where
they focused on alewife historic spawning habitat (lakes and ponds) and productivity rates
for the species, however they did not provide comparable estimates for blueback herring
and American shad, therefore we exclude the biomass reconstruction for these species under
the anadromous alosines group. Since 2013, NOAA’s National Marine Fisheries Service has
been committed to working with the Atlantic States Marine Fisheries Commission to fill
data gaps regarding the biology of alewives and blueback herring, yet aspects of blueback
herring ecology and biology remain unknown. We acknowledge that modeling a single spe-
cies in the anadromous alosine group is underestimating the full benefits of fish passage.
Nevertheless, this underestimation helps ensure that our results are conservative in scope.
Our analysis was motivated to understand the consequence of increasing alewife biomass in
The ecosystem modeling approach
We built two ecosystem models using the Ecopath with Ecosim framework (EwE 6.0, [35]) to
assess and quantify ecosystem-level biomass changes resulting from alosine biomass restora-
tion. Originally developed to address questions regarding ecosystem structure, dynamics and
external drivers, such as fishery harvest [3638], the mass-balance ecotrophic model represents
the ecosystem as functional groups or nodes (different species, ontogenetic phases or groups
with the same ecological importance) connected by trophic relationships. Our model, based
on Ecopath, the core routine of EwE, provides a static snapshot of a “closed” ecosystem, where
no imports with adjacent ecosystems were considered [39,40]. The links between the nodes
represent trophic interactions estimated from published diet studies. Thus, diet composition
determines energy and matter flow throughout the system in each time period. Ecopath’s
main equation takes the following form:
Pi¼BiM2iþYiþEiþBAiþPi ð1EEiÞ ð1Þ
where, for a given group (i), P
is production, B
is biomass, M2
is the total predation mortality
rate for group (i), Y
is the total fishery catch rate, E
is net-migration rate, BA
is biomass accu-
mulation rate for (i), EE
is ecotrophic efficiency (the proportion of the production used in the
system), and P
)represents the rate of other sources of mortality for (i) [41].
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 5 / 27
The following equation expresses the relationship between predator and prey:
j¼1ðBj ðQ=BÞjDCjiÞ ð2Þ
Where the biomass times the predation mortality of prey (i) equals the sum across all the pred-
ators (j) of the predator biomass B
times the consumption per unit biomass of (j)(Q/B)
the fraction of prey group (i) in the diet of predator group (j)DC
[42]. The Ecopath modeling
framework assumes that consumption equals production plus respiration and unassimilated
food. This equation is the representation of mass-balanced hypothesis.
These two main equations yield the following full linear equation for a given period. Eq 1
can be rewritten as:
Bi ðP=BÞiX
Bj ðQ=BÞjDCji  ðP=BÞiBi ð1EEiÞ  YiEiBAi¼0ð3Þ
Bi ðP=BÞiEEiX
Bj ðQ=BÞjDCji YiEiBAi¼0ð4Þ
where (P/B)
is the production of the functional group (i) per unit of biomass [35,4143].
The ecotrophic efficiency term EE
is solved by Eq 5:
EEi¼ ðYiþEiþBAiþM2iBiÞ=Pið5Þ
The ecotrophic efficiency varies between 0 and 1 and can be expected to approach 1 for
groups with high predation and exploitation pressures; this value is used here for tuning the
model. For groups where EE value is superior to 1, the remainder of parameters should be
tuned during the model parametrization, also known as the balancing process [41]. EwE’s mul-
tistanza function accounts for the ontogenetic differences between life stages. We first built
a fully balanced model using the multistanza approach. However, we forewent utilizing this
feature. Instead, we conserved ontogenetic groups as different nodes to simplify comparing
changes in biomass in the two models. To calculate production for each age node, we used the
following trophic and growth-based production model [44],
Where τis the trophic level (calculated by the first model using the multistanza approach from
diet data information), Kis the von Bertalanffy growth parameter of each species, and θis
water temperature, which we estimated using the mean temperature from each species’ spatial
range in the NEUS LME (Table E in S1 File). As described by the equations above, the Eco-
path’s main input parameters are B, P/B, Q/B, EE and diet regimes. Not all the parameters
used to construct an Ecopath model need to be entered; therefore missing parameters will be
estimated by the model using the balanced sets of equations.
Functional groups
The models were based on four EwE Models built for the Energy Modeling and Analysis eXer-
cise (EMAX) project [45,46] with the NOAA Northeast Fisheries Science Center (NEFSC)
data. The EMAX models presented an average of 36 functional groups per region, with low
taxonomic resolution. To create our baseline model (CAB), we averaged EMAX inputs and
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 6 / 27
expanded the functional groups to achieve higher taxonomic resolution. We separated key
ecological or economically important species into different ontogenetic groups and resulted in
a total of 59 functional groups (Table 1).
Model scenarios
We developed EwE models of the Northeast US LME to explore the potential marine ecosys-
tem effects of increasing anadromous alosine biomass by reestablishing full river to ocean con-
nectivity on the three Northern New England Watersheds: the Androscoggin, Kennebec, and
Penobscot river systems (total of 1.280 km
of lake/pond area). Both the Contemporary Alo-
sine Biomass Model (CAB) and the Restored Alosine Biomass Model (RAB) were built with
the same spatial structure, encompassing the full range of alewife (Fig 1) in the NEUS LME:
the Gulf of Maine, Georges Bank, Southern New England, and Middle Atlantic Bight (246,662
). However, RAB assumed restored alewife biomass based on historical landscape esti-
mates in Mattocks et al. [23], which resulted in a biomass input of 137,637 mt for the anadro-
mous alosine group. The CAB model anadromous alosine group biomass estimate used was
, while RAB estimate was 0.63
. Thus, it reflects the potential habitat expan-
sion on these Northern New England Watersheds (Fig 1).
Timeframe analysis
The models use the year block 2000 as the reference point for biomass, consumption, produc-
tion, diets, mortality and fishing mortality. This year block, comprising the years 1996 to 2000,
was chosen for use in the four EMAX Models due to the amount of available data.
Data sources
To build our baseline model of current conditions (CAB), we used sources including EMAX
Model raw input data, EMAX model balanced results, NEFSC trawl surveys, stock assess-
ments, and scientific literature. Our initial Ecopath parameter inputs (Biomass, Production,
Consumption, and Diets) came from weighted averages of the combined regions of the EMAX
models. Using these weighted averages, we calculated total biomass estimates for the Northeast
US LME area. The same process was applied to calculating production. Since consumption
was based on the amount of food ingested by a population relative to its biomass (in a given
year, [47]), the consumption biomass (Q/B) ratio was consistent among all EMAX regions. For
diet data, we used raw inputs from EMAX and from the Virginia Institute of Marine Science
Fish Food Habits database, which were modified during the balancing process (S1 File). Pre-
balancing was performed with PREBAL pre-balancing methodology [48] (Fig A in S1 File),
and balancing followed the guidelines in Heymans et al. [49]. Once the CAB model was bal-
anced, we generated the flow diagram (Fig 2) using the ecopath_matlab toolbox [50].
The model representing conditions without dams (RAB) was built in two steps. First, we
applied alewife historical productivity data based on landscape estimates that assumed full
river to ocean connectivity for the Northern New England Watersheds. These estimates were
derived from Mattocks et al. [23] and Hall et al. [28], who calculated declining alewife produc-
tion in lakes and ponds throughout New England from the year that dams began to obstruct
the rivers. The total lake/pond area (km
) and the total length of pre-dammed rivers provide
the total historical alewife spawning habitat (Fig 1). Both studies based habitat loss on species-
specific spawning habitat preferences. Since alewife prefers spawning in still water, we calcu-
lated total un-dammed lake and pond area in square kilometers (km
For the second step of the RAB model, we defined small pelagics and forage fish, and ana-
lyzed diet information to identify all functional groups that presented trophic interactions
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 7 / 27
Table 1. Functional groups input parameters sources for the Contemporary Alosine Biomass (CAB) model for the NEUS LME. Inputs parameters are Biomass (B),
the production-biomass ratio (P/B) and the consumption-biomass ratio (Q/B), output parameters calculated by EwE are Trophic level (TL), Ecotrophic Efficiency (EE)
and the production-consumption ratio (P/Q), signaled in bold. Input data documentation is found in the S1 File.
Node Group name TL B (
) P/B (y
) Q/B (y
) EE P/Q (y
1 Phytoplankton 1.00 20.13 180.69 0.58
2 Bacteria 2.00 3.83 91.25 182.50 0.88 0.50
3 Microzooplankton 2.22 3.16 72.00 242.42 0.54 0.30
4 Copepods S 2.10 7.81 42.58 127.75 0.98 0.33
5 Copepods L 2.23 7.63 48.52 109.50 0.90 0.44
6 Gelatinous Zooplankton 2.93 1.01 37.97 145.33 0.67 0.26
7 Micronekton 2.73 7.65 14.25 85.50 0.79 0.17
8 Macrobenthos polychaete 2.34 14.68 2.51 17.50 0.98 0.14
9 Macrobenthos crustaceans 2.62 5.90 3.06 21.00 0.79 0.15
10 Macrobenthos mollusks 2.28 8.34 2.04 13.95 0.94 0.15
11 Macrobenthos others 2.48 8.90 2.02 16.06 0.95 0.13
12 Megabenthos filters 2.11 3.00 3.94 16.51 0.20 0.24
13 Megabenthos others 2.97 4.50 1.90 9.53 0.63 0.20
14 Shrimp 2.80 1.96 1.00 5.00 0.50 0.20
15 Mesopelagic 3.27 0.15 0.65 1.83 0.75 0.36
16 Atlantic herring 3.51 6.20 0.62 4.59 0.61 0.14
17 Anadromous alosines 3.40 0.08 1.30 9.40 0.90 0.14
18 Atlantic menhaden S 2.50 1.58 1.50 15.86 0.54 0.09
19 Atlantic menhaden M 2.64 2.88 0.93 7.01 0.50 0.13
20 Atlantic menhaden L 2.78 0.49 0.90 4.38 0.86 0.21
21 Anchovies 3.70 2.32 3.00 10.90 0.76 0.28
22 Mackerel 3.83 0.77 0.39 1.98 1.00 0.20
23 Squid 3.71 1.06 0.98 2.70 0.83 0.36
24 Butterfish 3.59 0.90 1.27 1.98 0.42 0.64
25 Small pelagics 3.37 0.29 0.97 4.00 0.89 0.24
26 Bluefish S 4.36 0.05 0.51 18.11 0.94 0.03
27 Bluefish M 4.44 0.06 0.51 3.53 0.67 0.14
28 Bluefish L 4.64 0.19 0.49 1.93 0.14 0.25
29 Striped bass S 3.99 0.07 0.25 23.27 0.78 0.01
30 Striped bass M 4.05 0.37 0.25 6.35 0.19 0.04
31 Striped bass L 4.23 0.29 0.24 3.19 0.20 0.08
32 Weakfish S 4.07 0.16 0.45 13.52 0.92 0.03
33 Weakfish M 4.28 0.30 0.43 4.22 0.09 0.10
34 Weakfish L 4.35 0.04 0.42 2.45 0.48 0.17
35 Dogfish S 4.06 0.47 0.25 1.47 0.79 0.17
36 Dogfish L 4.09 2.70 0.24 0.61 0.07 0.40
37 Atlantic cod S 3.63 0.03 0.48 6.91 0.81 0.07
38 Atlantic cod M 3.92 0.08 0.46 3.49 0.96 0.13
39 Atlantic cod L 4.19 0.08 0.43 2.26 0.96 0.19
40 Haddock 3.69 0.60 0.45 3.00 0.45 0.15
41 Hake 3.81 0.83 1.12 3.85 0.64 0.29
42 Croaker 3.59 0.82 0.45 0.91 0.33 0.50
43 Yellowtail flounder S 3.60 0.04 1.07 4.41 0.17 0.24
44 Yellowtail flounder L 3.49 0.11 1.10 2.90 0.46 0.38
45 Summer flounder S 4.25 0.03 0.56 4.41 0.64 0.13
46 Summer flounder L 4.54 0.18 0.53 2.90 0.48 0.18
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PLOS ONE | May 23, 2019 8 / 27
with anadromous alosine and other forage fish groups. We used the ecotrophic efficiencies
from the CAB model to calculate new biomass estimates for the key functional groups that
incorporate the additional historical alewife biomass in the anadromous alosine group (Ale-
wife A.pseudoharengus, blueback herring A.aestivalis, and American shad A.sapidissima).
We analyzed the impacts on the marine environment of increasing forage fish biomass, in
the form of alewives (Alosa pseudoharengus) within the alosine functional group, by first calcu-
lating lost alosine productivity due to river impediment. Using methods in Mattocks et al.[23]
and Hall et al. [28], we estimated the potential young of the year (YoY) productivity. The aver-
age YoY alewife density in 18 ponds, determined by field surveys, was applied to the total
accessible pond and lake area for the three Northern New England watersheds,
where N
is the potential number of alewife YoY produced before emigration to the marine
habitat, D
is the YoY density of sampled lacustrine habitat (number of fish km
), and Ais
the total pond and lake area within watersheds.
An exponential model of population growth was used to estimate subsequent alewife year
to predict the abundance of alewives at years two, three and four. Nis the number of fish at
time t, and Zis the annual instantaneous (total) mortality rate of 0.8 [25]. After hatching, ale-
wives spend part of their first summer in their natal freshwater nursery habitat, and migrate to
coastal waters through the summer and fall of their first year [51,52]. Thus, we could estimate
total biomass using the resulting abundance and mean biomass at age (Tables J and K in S1
File). For fish in the 4+ age class, we used the mean weight shown in Hall et al. [28]. For other
age classes, we calculated weight using the fork length-weight (in grams) relationship [53],
W¼2:42 106FL3:34 ð9Þ
where FL (in mm) is fork length. FL data came from the Maryland Department of Natural
Resources (MDNR) in a long-term dataset collected since 1989.
Table 1. (Continued)
Node Group name TL B (
) P/B (y
) Q/B (y
) EE P/Q (y
47 Skate 3.83 1.66 0.45 2.40 0.29 0.19
48 Demersal benthivores 3.62 2.05 0.45 0.91 0.96 0.50
49 Demersal piscivores 4.13 0.55 0.55 1.21 0.95 0.45
50 Demersal omnivores 3.96 1.50 0.45 0.81 0.87 0.55
51 Medium pelagic 4.54 0.12 0.45 1.84 0.06 0.24
52 Coastal sharks 4.53 0.02 0.20 1.25 0.95 0.16
53 Pelagic sharks 4.59 0.02 0.11 0.69 0.32 0.16
54 Large pelagics (HMS) 4.31 0.07 0.58 6.79 0.83 0.09
55 Pinnipeds 4.49 0.04 0.08 5.50 0.25 0.01
56 Baleen whales 3.47 0.46 0.04 3.22 0.03 0.01
57 Odontocetes 4.49 0.06 0.04 14.30 0.60 0.00
58 Seabirds 4.27 0.01 0.28 9.32 0.42 0.03
59 Detritus 1.00 52.61 0.51
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PLOS ONE | May 23, 2019 9 / 27
Both models had 59 functional groups (S1 File) determined by ecological role and trophic
level. The Contemporary Alosine Biomass (CAB) model used biomass (B), consumption (Q/
B), production (P/B), and diets (DC) from stock assessments, NEFWS trawl survey, and fish- The model estimated Ecotrophic efficiency (EE). As input, the Restored Alosine Bio-
mass (RAB) model employed the potential alewife biomass of the Northern New England
Watersheds fully connected to the ocean. Using EE, P/B, Q/B as input parameters allowed
the model to calculate the biomass of various species of economic and conservation interest,
except for apex predator functional groups, for which EE approximated zero (Table 2) [49].
We verified our estimates by running the RAB model biomass outputs and alosine restored
biomass as our input parameters to confirm that we obtained the same EE for both models.
We assumed that the EE parameter for anadromous alosine would remain high after biomass
reconstruction for alewife, as they are a forage fish. During the balancing process for RAB
model, we modified the diets to account for the increase of anadromous alosine biomass. We
also increased the biomass for macrobenthos polychaetes, crustaceans and others to accommo-
date the increase in biomass of their predators (S1 File).
Niche overlap and ecological network analysis. Niche overlap analysis can describe a
variety of niche partitioning, in the EwE approach it is focused on the trophic relationships
[41]. We generated niche overlap plots focusing on the forage fish species, to evaluate how the
input of alosine biomass changes the niche for the group when compared to other species. The
niche overlap plots contrast and assign a degree of overlap by pairing species based on the tro-
phic interactions, and are given by prey overlap index, which shows whether the two groups
are consuming the same food resource, and predator overlap index, which demonstrates if the
two groups are preyed by same predators.
Ecological Network Analysis (ENA) is widely used to compare Ecopath models [49]. We
ran ENA to better understand the structure and function of the NEUS LME under contempo-
rary and restored anadromous alosine scenarios. These include trophic level decomposition
and keystoneness analysis.
The trophic level decomposition analysis breaks the continuous trophic levels of a func-
tional group into discrete trophic levels sensu Lindeman according to Ulanowicz’s approach
[35,54]. The analysis shows how many discrete trophic levels each functional group belongs to,
and the amount of biomass attributed to each discrete trophic level. It calculates the fractions
of the flow from each trophic level through each model group. For example, if an animal has
40% of its diet coming from primary producers, and 60% of it diet coming from first-order
carnivores, the corresponding fractions of the flow are attributed to both the herbivore and
first consumer levels [41]. We were particularly interested in what trophic level decomposition
analysis reveals about how biomass and energy flowed through the trophic network and how
biomass transfer differs between trophic levels in each scenario.
The “keystoneness index” refers to a continuous ranking of all functional groups according
to the importance of their proximity to a keystone role within the marine ecosystem [40]. All
groups present a degree of keystoneness. However, few have a keystone role in the ecosystem.
We ran a keystoneness analysis (KS
, [40]) comparing the two models to determine whether
the changes in biomass indicate differences in the keystone ranking of each functional group,
in particular the anadromous alosine.
In the RAB scenario, alosine biomass increased by 137,637 metric tons over the study area,
based on production from the three Northern New England watersheds assumed to be fully
connected to the sea (Table 3,Fig 3). Thirty-three of the functional groups’ biomasses were left
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 10 / 27
Table 2. Functional groups input parameters sources for the Restored Alosine Biomass (RAB) model for the NEUS LME. Inputs parameters are the production-bio-
mass ratio (P/B), the consumption-biomass ratio (Q/B), and Ecotrophic Efficiency (EE) from CAB model. Output parameters calculated by EwE are Trophic level (TL),
Biomass (B) and the consumption-production ratio (P/Q), signaled in bold.
Node Group name TL B (
) P/B (y
) Q/B (y
) EE P/Q (y
1 Phytoplankton 1.00 20.13 180.69 0.58
2 Bacteria 2.00 3.83 91.25 182.5 0.90 0.50
3 Microzooplankton 2.22 3.16 72.00 242.42 0.55 0.30
4 Copepods S 2.10 7.81 42.58 127.75 0.82 0.33
5 Copepods L 2.23 7.63 48.52 109.50 0.92 0.44
6 Gelatinous Zooplankton 2.93 1.01 37.97 145.33 0.69 0.26
7 Micronekton 2.62 7.65 14.25 85.50 0.85 0.17
8 Macrobenthos polychaete 2.33 14.92 2.51 17.50 0.93 0.14
9 Macrobenthos crustaceans 2.55 6.30 3.06 21.00 1.00 0.15
10 Macrobenthos mollusks 2.28 8.34 2.04 13.95 0.84 0.15
11 Macrobenthos others 2.47 9.39 2.02 16.06 0.79 0.13
12 Megabenthos filters 2.11 3.00 3.94 16.51 0.23 0.24
13 Megabenthos others 2.87 4.50 1.90 9.53 0.80 0.20
14 Shrimp 2.78 3.02 1.00 5.00 0.50 0.20
15 Mesopelagic 3.25 0.27 0.65 1.83 0.75 0.36
16 Atlantic herring 3.44 10.41 0.62 4.59 0.61 0.14
17 Anadromous alosines 3.36 0.63 1.30 9.40 0.90 0.14
18 Atlantic menhaden S 2.50 2.02 1.50 15.86 0.54 0.09
19 Atlantic menhaden M 2.64 3.39 0.93 7.01 0.50 0.13
20 Atlantic menhaden L 2.78 0.84 0.90 4.38 0.86 0.21
21 Anchovies 2.98 3.28 3.00 10.90 0.76 0.28
22 Mackerel 3.68 1.16 0.39 1.98 1.00 0.20
23 Squid 3.64 2.10 0.98 2.70 0.83 0.36
24 Butterfish 3.56 0.90 1.27 1.98 0.88 0.64
25 Small pelagics 3.32 0.69 0.97 4.00 0.89 0.24
26 Bluefish S 3.94 0.05 0.51 18.11 0.94 0.03
27 Bluefish M 4.13 0.06 0.51 3.53 0.67 0.14
28 Bluefish L 4.49 0.19 0.49 1.93 0.14 0.25
29 Striped bass S 3.72 0.08 0.25 23.27 0.78 0.01
30 Striped bass M 3.84 0.37 0.25 6.35 0.19 0.04
31 Striped bass L 3.98 0.29 0.24 3.19 0.20 0.08
32 Weakfish S 3.74 0.21 0.45 13.52 0.93 0.03
33 Weakfish M 3.86 0.30 0.43 4.22 0.11 0.10
34 Weakfish L 3.97 0.04 0.42 2.45 0.49 0.17
35 Dogfish S 4.01 0.80 0.25 1.47 0.79 0.17
36 Dogfish L 4.04 2.70 0.24 0.61 0.15 0.40
37 Atlantic cod S 3.57 0.07 0.48 6.91 0.81 0.07
38 Atlantic cod M 3.87 0.15 0.46 3.49 0.97 0.13
39 Atlantic cod L 4.14 0.18 0.43 2.26 0.96 0.19
40 Haddock 3.64 0.60 0.45 3.00 0.61 0.15
41 Hake 3.71 1.25 1.12 3.85 0.64 0.29
42 Croaker 3.53 0.82 0.45 0.91 0.38 0.50
43 Yellowtail flounder S 3.54 0.04 1.07 4.41 0.25 0.24
44 Yellowtail flounder L 3.46 0.11 1.10 2.90 0.47 0.38
45 Summer flounder S 4.07 0.09 0.56 4.41 0.64 0.13
46 Summer flounder L 4.37 0.40 0.53 2.90 0.48 0.18
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PLOS ONE | May 23, 2019 11 / 27
to be estimated by RAB model (Table 2), resulting in 3,603,452 metric tons increase in total
biomass over the CAB model, excluding the alosine biomass input. Impacted species were
grouped in broader categories as follow: forage species, piscivorous fish, invertebrates and ver-
tebrates (sharks and other species of conservation concern). Besides the anadromous alosine
group, the forage species category included mesopelagics (e.g. Maurolicus sp.), Atlantic her-
ring, the three size classes of Atlantic menhaden (Brevoortia tyrannus), anchovies (e.g. Ancho
sp.), Atlantic mackerel (Scomber scombrus), butterfish (Peprilus triacanthus), and other small
pelagics (e.g. Ammodytes sp.). Butterfish was the only forage species in RAB which the biomass
was not calculated by the RAB model (Table 2). For the entire forage species, there was total
biomass increase of 1,957,052 metric tons or 50.7%.For both models the forage species groups
with the greatest niche overlap where anadromous alosine, other small pelagics, and the three
menhaden age classes (Fig 4). There was a considerable shift towards a higher predator overlap
index in the RAB model, which was observed among a number of species with the anadro-
mous alosine group (Fig 4). The RAB model indicates stronger predator overlap between
anadromous alosines and Atlantic herring, medium and large menhaden, and mesopelagics,
demonstrating the potential food base for the main apex predators.
For piscivorous species, including economically important Atlantic cod and summer floun-
der (Paralichthys dentatus), biomass potentially increased by 26.6%, the equivalent of 875,113
metric tons (Table 3,Fig 3). Cod was divided into three size classes, small (20 cm total
length), medium (21–50 cm), and large (>50 cm), to account for ontogenetic stages. Cod
biomass increased for all three size groups, but large cod increased the most in the alosine
biomass restoration scenario (22,438 mt)––this is roughly equivalent to the entire Gulf of
Maine spawning stock biomass from 1980 to 1990 [55]. In addition to changing temperature,
another limitation for cod populations is an energetic bottleneck that occurs after age four
(large cod >50 cm), when their shift from a benthic to a pelagic diet caps productivity [56].
Our model suggests that increasing the forage fish base would directly benefit large cod by
opening up the bottleneck.
From the invertebrates groups, the RAB model was set to calculate the biomasses for shrimp
and squid functional groups, while for macrobenthos and megabenthos we provided the bio-
mass values (S1 File for the list of species). The squid functional group composed by longfin
inshore squid (Doryteuthis pealeii) and northern shortfin squid (Illex illecebrosus), had an
Table 2. (Continued)
Node Group name TL B (
) P/B (y
) Q/B (y
) EE P/Q (y
47 Skate 3.76 1.66 0.45 2.40 0.43 0.19
48 Demersal benthivores 3.54 2.62 0.45 0.91 0.96 0.50
49 Demersal piscivores 4.05 0.85 0.55 1.21 0.95 0.45
50 Demersal omnivores 3.89 2.84 0.45 0.81 0.87 0.55
51 Medium pelagic 4.45 0.12 0.45 1.84 0.07 0.24
52 Coastal sharks 4.41 0.02 0.20 1.25 0.95 0.16
53 Pelagic sharks 4.49 0.05 0.11 0.69 0.32 0.16
54 Large pelagics (HMS) 4.06 0.07 0.58 6.79 0.83 0.09
55 Pinnipeds 4.36 0.06 0.08 5.50 0.25 0.01
56 Baleen whales 3.43 0.46 0.04 3.22 0.04 0.01
57 Odontocetes 4.34 0.46 0.04 14.30 0.60 0.003
58 Seabirds 4.23 0.01 0.28 9.32 0.42 0.03
59 Detritus 1.00 52.61 0.53
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PLOS ONE | May 23, 2019 12 / 27
Table 3. Differences in biomass between the CAB and RAB models.
Node Group name CAB Biomass in habitat
area (t/km
CAB Biomass
RAB Biomass in habitat
area (t/km
RAB Biomass
Difference between
models (mt)
Rate of increase
1 Phytoplankton 20.13 4965306 20.13 4965306 no change -
2 Bacteria 3.83 943975 3.83 943975 no change -
3 Microzooplankton 3.16 779699 3.16 779699 no change -
4 Copepods S 7.81 1926184 7.81 1926184 no change -
5 Copepods L 7.63 1882771 7.63 1882771 no change -
6 Gelatinous
1.01 249869 1.01 249869 no change -
7 Micronekton 7.65 1887951 7.65 1887951 no change -
8 Macrobenthos
14.68 3621491 14.92 3680197 58705.556 1.6
9 Macrobenthos
5.90 1454319 6.30 1552984 98664.8 6.8
10 Macrobenthos
8.34 2057161 8.34 2057161 no change -
11 Macrobenthos others 8.90 2195045 9.39 2316132 121086 5.5
12 Megabenthos filters 3.00 739246 3.00 739246 no change -
13 Megabenthos others 4.50 1109486 4.50 1109486 no change -
14 Shrimp 1.96 483458 3.02 744499 261042 54.0
15 Mesopelagic 0.15 37246 0.27 67672 30426 81.7
16 Atlantic herring 6.20 1528349 10.41 2568447 1040098 68.1
17 Anadromous alosines 0.08 18746 0.63 156384 137637 734.2
18 Atlantic menhaden S 1.58 389953 2.02 497511 107557 27.6
19 Atlantic menhaden M 2.88 709874 3.39 835916 126042 17.8
20 Atlantic menhaden L 0.49 120376 0.84 206011 85635 71.1
21 Anchovies 2.32 572244 3.28 808649 236404 41.3
22 Mackerel 0.77 190916 1.16 285025 94108 49.3
23 Squid 1.06 261955 2.10 517432 255477 97.5
24 Butterfish 0.90 221502 0.90 221502 no change -
25 Small pelagics 0.29 71532 0.69 170676 99144 138.6
26 Bluefish S 0.05 11100 0.05 13444 2344 21.1
27 Bluefish M 0.06 14553 0.06 15160 607 4.2
28 Bluefish L 0.19 47606 0.19 47930 324 0.7
29 Striped bass S 0.07 16325 0.08 19978 3653 22.4
30 Striped bass M 0.37 90113 0.37 91250 1138 1.3
31 Striped bass L 0.29 71047 0.29 72099 1052 1.5
32 Weakfish S 0.16 38233 0.21 52428 14195 37.1
33 Weakfish M 0.30 74739 0.30 74739 no change -
34 Weakfish L 0.04 8880 0.04 8880 no change -
35 Dogfish S 0.47 116295 0.80 197361 81066 69.7
36 Dogfish L 2.70 665987 2.70 665987 no change 0.0
37 Atlantic cod S 0.03 6559 0.07 18429 11870 181.0
38 Atlantic cod M 0.08 20620 0.15 36221 15602 75.7
39 Atlantic cod L 0.08 20801 0.18 43216 22416 107.8
40 Haddock 0.60 148737 0.60 148737 no change -
41 Hake 0.83 203989 1.25 308565 104575 51.3
42 Croaker 0.82 201210 0.82 201210 no change -
43 Yellowtail flounder S 0.04 10827 0.04 10827 no change -
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PLOS ONE | May 23, 2019 13 / 27
increase of 97.5%, the equivalent of 255,477 metric tons. For the shrimp group, there was an
increase of 54% or 261,041 metric tons.
Species of conservation concern benefitted from the augmented forage base. Toothed
whales, pinnipeds, pelagic sharks and seabirds, together, showed a biomass increase of 69% or
113,948 metric tons. Toothed whales (Odontocetes) alone would potentially increase by 99,177
metric tons. The contrast between the CAB and RAB models trophic level decompositions
shows the magnitude of the change in biomass flows between the scenarios. The trophic level
decomposition analysis shows the difference in biomass flows from each discrete trophic level
and illustrates the differences in the magnitude of the trophic composition of species of conser-
vation concern in NEUS LME, and how the new biomasses increase the allocation of the frac-
tions of the flow. We separated key functional groups to present the magnitude of energy flow
changes attributed to increased anadromous alosine biomass, and how the restoration of
only a few rivers promotes additional production across multiple key species (Fig 5,Table 4).
Table 4 shows the allocations’ differences between CAB and RAB models, used to generate
Fig 5.
The keystoneness analysis, a measure of network connectivity, also revealed differences
between the two models. For the CAB model, the top five species ranked from highest to low-
est on the keystone index were: micronekton (0.044), macrobenthos crustaceans (0.017),
coastal sharks (0.0039,), large copepods (0.0032) and phytoplankton (-0.041). The RAB
model’s first- and second-ranked functional groups were the same as the CAB model (micro-
nekton = 0.00668, and macrobenthos crustaceans = -0.00124); however, large copepods
(-0.00389) and phytoplankton (-0.0393) occupied the third and fourth places, respectively,
and Odontocetes (-0.0463) occupied fifth place (Fig 5). Among the groups under the forage
fish category, the anadromous alosine group was the one that showed the most considerable
changes in keystoneness index, increasing twelve positions on the rank, from fifty-third
place on CAB to forty-first place on RAB model. Anchovies were the component of the for-
age fish species that ranked the highest, with a rise of two steps on the keystoneness ranking
= -0.123 [rank 8], and RAB KS
= -0.067 [rank 6]). Atlantic herring also showed a
Table 3. (Continued)
Node Group name CAB Biomass in habitat
area (t/km
CAB Biomass
RAB Biomass in habitat
area (t/km
RAB Biomass
Difference between
models (mt)
Rate of increase
44 Yellowtail flounder L 0.11 27417 0.11 27417 no change -
45 Summer flounder S 0.03 7385 0.09 21288 13904 188.3
46 Summer flounder L 0.18 43273 0.40 97531 54258 125.4
47 Skate 1.66 408226 1.66 408226 no change -
48 Demersal benthivores 2.05 506644 2.62 646985 140341 27.7
49 Demersal piscivores 0.55 134677 0.85 210712 76035 56.5
50 Demersal omnivores 1.50 369993 2.84 701726 331733 89.7
51 Medium pelagic 0.12 29846 0.12 29846 no change -
52 Coastal sharks 0.02 4415 0.02 4620 204 4.6
53 Pelagic sharks 0.02 3947 0.05 11233 7287 184.6
54 Large pelagics (HMS) 0.07 17266 0.07 17401 135 0.8
55 Pinnipeds 0.04 8633 0.06 14516 5883 68.1
56 Baleen whales 0.46 114451 0.46 114451 no change -
57 Odontocetes 0.06 14800 0.46 113977 99177 670.1
58 Seabirds 0.01 1727 0.01 2989 1262 73.1
59 Detritus 52.61 12975694 52.61 12975694 no change -
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PLOS ONE | May 23, 2019 14 / 27
rank increase of two steps, shifting from the fifteenth position to thirteenth (CAB KS
-0.23, and RAB KS
= -0.201) (Fig 6).
The Restored Alosine Biomass model offers a “what if” scenario of potential benefits to NEUS
LME due to increased connectivity between rivers and oceans. Since anadromous alosine
group depletion is acknowledged and its restoration is an active management goal, modeling
the potential ecological benefits of much larger alewife populations will inform ongoing efforts.
Our approach incorporated EE parameters from the CAB model to generate biomass potential
for functional groups that have trophic interactions with the anadromous alosine group. Our
results, based solely on alewife biomass changes, highlights the species importance as a compo-
nent of the forage fish complex. This effort represents the first-time historical landscape-based
estimates of an anadromous fish species were used to inform a marine ecosystem model.
Increasing overall forage group biomass promoted energy flow through the mid-trophic levels
to the benefit of numerous functional groups, demonstrating the enhanced potential of ecosys-
tems with river-ocean connectivity. Ongoing efforts to advance understanding of ecosystem
connectivity should be encouraged, due to the widespread positive impacts in the current
Fig 3. Comparing biomass of functional groups benefiting from alosine restoration. Contemporary and restored
biomass for all functional groups impacted by alosine biomass restoration. The y-axis was square transformed to show
differences for functional groups with low biomass. Groups that presented biomass change less than to 0.002
were dropped from the graph. Age groups are represented by size, as small (S), medium (M), and large(L).
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 15 / 27
Fig 4. Niche overlap index plot of the forage fish functional groups. (A) Contemporary Alosine Biomass model. (B)
Restored Alosine Biomass model. The color gradient and size of nodes are representing the predator overlap index
number. Numbers refer to the functional groups, anadromous alosine are represented by underlined numbers.
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 16 / 27
Keystone species are essential drivers of ecosystem processes and can impose limits on
other species through predation or resource partitioning. Predators have more substantial
ecosystem impacts relative to their biomass and drive top-down control of the system [57].
Comparing the RAB and CAB models the top keystone species remained similar, with the
downgrading of coastal sharks and upgrading of odontocetes (dolphins, porpoises and sperm
whales). In Newfoundland, the Mediterranean and the Eastern Pacific odontocetes also rank
high on the keystoneness index [40,58,59]. Coll et al. [58] attribute the group’s significance to
Fig 5. Trophic level decomposition of key species in the Northeast US marine ecosystem. Roman numerals represent the discrete trophic
levels of the functional groups in the Contemporary Alosine Biomass (CAB) and Restored Alosine Biomass (RAB) models. (A) Large Atlantic
cod, Gadus morhua. (B) Large summer flounder, Paralichthys dentatus. (C) Pelagic sharks, Sphyrna sp., Carcharodon Carcharias,Prionace
glauca,Isurus sp., Lamna nasus, and Alopias vulpinus. (D) Pinnipeds, Phoca vitulina,Halichoerus grypus,Pagophilus groenlandicus, and
Cystophora cristata. (E) Odontocetes, Delphinus delphis,Globicephala sp., Grampus griseus,Kogia sp., Lagenorhynchus acutus,Phocena phocena,
Physeter macrocephalus,Stenella coeruleoalba,S.frontalis,Tursiops truncatus,Ziphius sp. (F) Seabirds, Calonectris diomedae,Fulmarus glacialis,
Larus marinus,L.argentatus,L.philadelphia,Oceanites oceanicus,Phalaropus fulicarius,Puffinus gravis,P.griseus,Rissa tridactyla,Sula
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 17 / 27
its non-exploited status. Anadromous alosines group had the second highest ranking increase,
highlighting how the group’s ecosystem roles were shuffled as their abundance waxes. In both
scenarios, phytoplankton and zooplankton components, such as micronekton and copepods,
ranked high in keystoneness (Fig 6). Other models [1,2] have demonstrated the pervasive
influence of seasonal phytoplankton regimes in temperate and coastal ecosystems such as the
Gulf of Maine and the Chesapeake Bay.
Regardless, the approach allows assessment of how alosines are connected to broader eco-
system functioning through trophic relationships, and offers a perspective on how increases in
the contribution of forage fish will impact top predators and energy flows [60]. Previous stud-
ies point out that different dynamics are possible in ecosystems, such as top-down, bottom-up
control, and wasp waist fishery dynamics [61]. Although none of the groups of the forage fish
Table 4. The difference in trophic level decomposition (sensu Lindeman) between the CAB and RAB models.
Discrete trophic level (
Id. Functional group Species II III IV V VI VII VIII IX
(A) Atlantic Cod L Gadus morhua 0.045 0.113 0.041 0.007 0.001
(B) Summer flounder L Paralichthys dentatus 0.106 0.333 0.164 0.031 0.005 0.001
(C) Pelagic sharks Alopias vulpinus 0.002 0.008 0.007 0.002
Carcharodon carcharias
Isurus sp.
Lamna nasus
Prionace glauca
Sphyrna sp.
(D) Pinnipeds Cystophora cristata 0.001 0.026 0.067 0.032 0.006 0.001
Halichoerus grypus
Pagophilus groenlandicus
Phoca vitulina
(E) Odontocetes Delphinus delphis 0.790 2.991 1.576 0.337 0.053 0.007 0.001
Globicephala spp.
Grampus griseus
Kogia spp.
Lagenorhynchus acutus
Phocena phocena
Physeter macrocephalus
Stenella coeruleoalba
Tursiops truncatus
Ziphius spp.
(F) Seabirds Calonectris diomedae 0.008 0.027 0.011 0.002 0.001
Fulmarus glacialis
Larus marinus
Oceanites oceanicus
Phalaropus fulicarius
Puffinus gravis
Rissa tridactyla
Sula bassanus
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PLOS ONE | May 23, 2019 18 / 27
Fig 6. Keystoneness analysis for both models using KS
index. The functional group lists are ranked and ordered in terms of
keystoneness, and circle size reflects biomass. (A) Keystoneness and biomass for the CAB, (B) keystoneness and biomass for the
RAB model. Forage fish species are highlighted in red, and anadromous alosine group is in bold.
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 19 / 27
complex are considered marine keystone species, their role in energy transfer is relevant to the
functioning of the NEUS LME. An order of magnitude change in alosine biomass positively
drove potential flow to species of economic and conservation concern. In an ecosystem, several
variables can also affect biomass fluctuations including climate fluctuations, fishing pressure,
geographic dispersal of species and changes in productivity pulses that were not accounted for
in this simulation and would have to be considered when operationalizing such models for
ecosystem-based fisheries management. To do so will require a perspective that includes both
the connectivity to freshwater ecosystems and the historical productivity estimates, if the full
potential of fisheries is expected.
Current river herring stocks are but remnants of historically abundant and widespread pop-
ulations [25]. Their absence from coastal ecosystems contributes to a niche-specific bottleneck
in pelagic mid-trophic forage species group. As climate change places more energetic demands
on predator populations, loss of functional redundancies in prey populations will become even
more problematic as the remaining forage species undergo natural fluctuations [7,16]. In
diverse ecological communities, seasonal pulses of prey species with different life histories pro-
vide stable food for apex predators (Fig 7A). This portfolio [62] effect no longer appears to
function in the Gulf of Maine, which has become heavily reliant on Atlantic herring, and pred-
ators likely suffer higher energetic costs during periods of low Atlantic herring abundance (Fig
7B). In addition to the impacts on the marine environment, the loss of connectivity also affects
riverine [23] and estuarine systems. There is evidence that juvenile planktivorous, such as
Atlantic herring and sand lance are more dominant food base than river herring in the estuary
of Saco River [63], a heavily dammed watershed, adjacent to the watersheds of our study.
Atlantic herring stock projections show a high likelihood of overfished and overfishing status
in the future, due to sustained low recruitment since 2011 [64]. This raises concern for the sus-
tainability of the forage base and their fisheries in the Gulf of Maine.
Stabilizing the forage fish portfolio requires re-establishing species diversity across the eco-
system. We acknowledge the likelihood that fish stocks will continue to be managed individu-
ally, yet our work emphasizes that even depleted stocks are critical to the forage fish pool [65].
Restoring diversity requires restoring connectivity across the entire spatiotemporal patchwork.
Managing the pelagic forage complex as a group is analogous to the current groundfish frame-
work, which considers co-occurring species with separate assessments but with a recognition
of similarities in habitat-use, fisheries catch and functional roles in the ecosystem.
Large fluctuations in fish populations have led to the assumption that populations always
self-replenish along taxa-specific time scales [66]. Marine clupeids are more likely to experi-
ence population recovery on shorter timescales than gadids and other marine fishes [66], and
one would think that small pelagic anadromous fish are the same. However, lack of population
recovery for clupeids stocks such as American shad and river herring suggests that resilience
of the anadromous forage fish complex has been overestimated concerning the multiple
impacts they face [67].
Despite recognizing the importance of the forage group as a vector of energy to higher tro-
phic levels, there is a lack of understanding of the spatial-temporal dynamics of different forage
species. Currently, small pelagics account for 30% of global fisheries landings. Atlantic herring
and menhaden yield the highest landings among all fish species in the Northeast United States
[68]. They support several fisheries sectors, including the bait, feed, and oil reduction and
extraction industries. However, rates of forage fish exploitation are raising red flags as their
depletion is linked to the poor body condition, decreased fecundity, impeded recovery, and
threatened the survival of a wide range of species [1,69]. Coastal and anadromous species are
important constituents of the forage fish group, as we have demonstrated, yet they have experi-
enced even higher rates of decline [70]. The functional removal of Atlantic herring in the
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 20 / 27
1970s [71], following declines in river herring and Atlantic menhaden, would have consider-
ably strained remaining forage populations, such as sand lance [72].
Hilborn et al. [15] point out that predators often have flexibility in foraging; only 10% of
predator populations are directly linked to a single prey species. We find that the MAB region
is more likely to promote generalist diets than the GOM. As a result, natural fluctuations in
Fig 7. Contrasting forage fish biomass time series in two Northeast US sub-regions. (A) In the Middle Atlantic
Bight (MAB), the total forage fish biomass trend is driven by similar fluctuations within several different forage fish
stocks. (B) In the Gulf of Maine (GOM), the total forage fish biomass trend is mostly driven by Atlantic herring (green
line) fluctuations. Biomass data is from NEFSC trawl surveys, 1963 to 2013, with corrected catchability (q).
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 21 / 27
forage fish abundance [65,73] in MAB are more easily offset by redundancy in the forage base
than in the GOM, where predators have become dependent on Atlantic herring (Fig 7).
McClatchie et al. [73] show that, despite naturally fluctuating cycles of the three main forage
species pre-exploitation, their aggregate biomass held constant. Unfortunately, most diet infor-
mation aggregated [74] and collected over a limited seasonal period. Thus, seasonal depen-
dence on specific forage species is often underestimated. However, there are plenty of
examples of species that heavily rely on short bursts of single prey species [9,17,75]. A new par-
adigm is emerging, which considers spatial and temporal variations in the forage base, and
contrasts availability versus food quality in predator diets. Simplified food web models and
diet aggregations can underestimate the importance of forage fish in food webs [76], and
scarce information may limit the successful application of management policies intended to
provide a more holistic approach. The value of alosine clupeids is made even greater by their
niche overlap, making them a flexible food item for many species at specific times and places.
Restored watersheds with incentivized dam removal and fish passage policies will raise the
capacity of resilience of anadromous forage fish populations. Applying these measures, we can
once again provide the benefits of the successful anadromous life history strategy that became
disadvantaged with anthropogenic modifications to the environment [67]. We acknowledge
that dam removal should be examined as a case by case, weighing the trade-offs that might
occur from removing the services associated with the dams [77]. Here we quantified the poten-
tial of river restoration and tested the potential biomass flow increase in marine food webs. We
highlight the historical role of rivers in marine ecosystem functioning through anadromous for-
age fish, a group that requires a myriad of habitats to support their life history strategies [67].
We acknowledge that there is no way back to Neverland, or to past conditions, as changes
in the physical system guide biological process away from the reference points [78]. However,
we should consider historical baselines to avoid the use of already impacted populations and
ecosystems reference points and parameters to identify targets for rehabilitation measures, the
essence of shifting baseline syndrome [79], and establish a clear path towards management
goals. In the end, our motivation to perform the current study came from centuries of histori-
cal accounts of the importance of alewife schools in attracting highly priced “good fish” [80].
Ongoing efforts to advance understanding of ecosystem connectivity should be encouraged.
Moving forward, a continued conversation regarding all the factors that influence alosine
recovery, and other coastal forage populations, and what the ecosystem implications are within
a temporal and spatial framework is required for a more holistic approach to managing these
coupled natural-human systems.
Supporting information
S1 File. Model documentation. Table and figures for all taxa components of the functional
groups and their respective data sources of the NEUS LME.
S1 Table. Contemporary Alosine Biomass (CAB) model diet matrix.
S2 Table. Restored Alosine Biomass (RAB) model diet matrix.
We would like to thank the crew and staff of the Northeast Fisheries Science Center trawl sur-
veys, and particularly Sean Lucey, for providing biomass and diet information. We acknowledge
Connectivity strengthens marine food webs
PLOS ONE | May 23, 2019 22 / 27
the Virginia Institute of Marine Sciences for sharing diet data. We would like to acknowledge
the work of all the scientists involved in the Energy Modeling and Analysis eXercise (EMAX)
for giving us the start point to complete this work. We also would like to thank and NMFS and
ASMFC working groups who developed population estimates. Howard Townsend provided key
support. Andre Buchheister and Thomas J. Miller provided key input for the first stages of the
analysis process. Karen Alexander for the essential input on the final stage of the manuscript.
Dr. Karin Limburg, Dr. Ge
´raldine Lassalle and one anonymous reviewer for their constructive
comments and discussions that improved the manuscript. Finally, we would like to thank Villy
Christensen, for sharing his knowledge regarding ecosystem modeling.
Author Contributions
Conceptualization: Beatriz S. Dias, Adrian Jordaan.
Data curation: Beatriz S. Dias.
Formal analysis: Beatriz S. Dias.
Funding acquisition: Adrian Jordaan.
Methodology: Beatriz S. Dias, Michael G. Frisk, Adrian Jordaan.
Supervision: Adrian Jordaan.
Validation: Beatriz S. Dias.
Visualization: Beatriz S. Dias.
Writing – original draft: Beatriz S. Dias, Michael G. Frisk, Adrian Jordaan.
Writing – review & editing: Beatriz S. Dias, Michael G. Frisk, Adrian Jordaan.
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... relatively frequent sharp collapses and fast recoveries (Lindegren et al. 2013). Fluctuations in the abundance of forage fish have been directly related to marine ecosystem regime shifts (Auber et al. 2015), and resilience (Dias et al. 2019). Given the importance of forage fish to marine ecosystem functioning, fisheries exploitation, and ecosystem-based management approaches (Francis et al. 2007), linking their population dynamics through time to the broader ecosystem is essential for understanding consequences of management decisions. ...
... The Northeast US continental shelf large marine ecosystem, particularly the Gulf of Maine, is among the most productive and biodiverse marine temperate areas in the world (Sherman and Skjoldal 2002;Overholtz and Link 2006). Forage fish, which are composed of anadromous and oceanodromous species with distinct life history traits, are an important component of the Gulf of Maine food webs and fisheries productivity (Dias et al. 2019). The former spends most of their life in the ocean followed by migration into freshwater to reproduce, contrasting a fully marine life history. ...
... sapidissima), which have experienced long-term declines primarily associated with high fisheries removals, including incidental catch or bycatch, and loss of spawning habitat (Limburg and Waldman 2009). While anadromous forage fish remain in the contemporary Gulf of Maine ecosystem, their role and abundance has been greatly reduced (Limburg and Waldman 2009;Dias et al. 2019). In addition, oceanodromous species such as Atlantic herring are the focus of largescale fisheries and have experienced large fluctuations in population size that undercuts system resilience to future change and exploitation which particularly impacts regions like the Gulf of Maine with low forage fish diversity (Dias et al. 2019). ...
Full-text available
Small pelagics, or forage fish, link lower and higher trophic levels in marine food webs. Recently, attention has been given to the management of forage fish, including anadromous river herring (Alewife Alosa pseudoharengus, blueback herring A. aestivalis) and American shad (A. sapidissima) due to their current depleted status and historically important ecological and economic roles. Little is known about the impact of changes in their biomass on marine food webs and what management practices will promote their recovery. Estimated historical riverine productivity was utilized to evaluate potential ecosystem impacts of the increasing river to ocean connectivity to resemble 19th‐century conditions. The Ecopath with Ecosim modeling framework was used to simulate management strategies, focused on anadromous forage fish, by creating scenarios of fisheries reduction (mixed fishery effort reduction) and river to ocean habitat connectivity (75% of historical connectivity achieved). Sixty‐year simulations covered the entire time series including a 36‐year forecast period to evaluate the ecosystem impacts of management strategies. Results suggest nonlinear relationships and large changes in biomass flows from forage fish to upper trophic levels in the Gulf of Maine ecosystem. Increases in biomass were observed for pelagic sharks, demersal piscivores, and species of conservation concern such as pinnipeds and seabirds, although overall results were strongly influenced by indirect trophic effects. Promoting anadromous forage fish recovery through increased connectivity resulted in the redundancy of marine ecosystem niches that would increase resilience to climate, fisheries, and other perturbations. This study highlights the value of employing ecosystem models for testing management scenarios to contrast different approaches to recover anadromous forage fish towards its former ecological prominence.
... Furthermore, evidence for differential growth and accumulation of energy reserves along a seasonality gradient indicate that environmental factors drive evolution in energy allocation strategies (Schultz et al., 1998;Schultz & Conover, 1997). High lipid prey species are particularly important in food webs, and their inclusion and exclusion from a functional ecosystem role can have system-wide influence (Dias et al., 2019;Österblom et al., 2008). Some species undergo ontogenetic shifts that place additional constraints on growth, perhaps none more so than species that undergo migrations such as diadromous fishes. ...
... If suboptimal conditions lead to smaller, less energy-dense individuals, less energy will be available for upper trophic levels, leading to lowered condition and productivity in predator species (Rand et al., 1994). At landscape scales, these impacts could alter food web energy flow in coastal ecosystems (Dias et al., 2019). ...
... A. pseudoharengus are a keystone species, driving increased productivity by providing energy and nutrients to freshwater and marine environments (Dias et al., 2019;Durbin et al., 1979;Hanson & Curry, 2005;Mattocks et al., 2017;Walters et al., 2009). Their designation as a Species of Concern and candidacy for an Endangered Species listing has driven habitat restoration efforts to target fish passage and dam removals. ...
Growth rate and energy reserves are important determinants of fitness and are governed by endogenous and exogenous factors. Thus, examining the influence of individual and multiple stressors on growth and energy reserves can help estimate population health under current and future conditions. In young anadromous fishes, freshwater habitat quality determines physiological state and fitness of juveniles emigrating to marine habitats. We tested how temperature and food availability affect survival, growth, and energy reserves in juvenile anadromous alewives (Alosa pseudoharengus), a forage fish distributed along the eastern North American continent. Field-collected juvenile anadromous A. pseudoharengus were exposed for 21 days to one of two temperatures (21°C and 25°C) and one of two levels of food rations (1% or 2% tank biomass daily) and compared for differences in final size, fat mass-at-length, lean mass-at-length, and energy density. Increased temperature and reduced ration both led to lower growth rates and the effect of reduced ration was greater at higher temperature. Fat mass-at-length decreased with dry mass and energy density increased with total length, suggesting size-based endogenous influences on energy reserves. Lower ration also directly decreased fat mass-at-length, lean mass-at-length and energy density. Given the fitness implications of size and energy reserves, temperature and food availability should be considered important indicators of nursery habitat quality and incorporated in A. pseudoharengus life history models to improve forecasting of population health under climate change. This article is protected by copyright. All rights reserved.
... Blueback herring populations remain at historically low levels, likely due to a combination of overfishing, habitat loss, predation and climate change (Davis et al., 2012;Hall et al., 2011;Schmidt et al., 2003). Thus, blueback herring are a target of ongoing restoration efforts because of the critical role they, and the congeneric species alewife (Alosa pseudoharengus), hold as an abundant lipid-rich resource for aquatic and terrestrial life in coastal and oceanic environments (Dias et al., 2019;Durbin et al., 1979;Walters et al., 2009). Several studies have identified the relative importance of adult blueback herring population sizes, density dependence and abiotic factors on juvenile abundance (Devine et al., 2021;Kosa and Mather, 2001;Tommasi et al., 2015), but there is little mechanistic understanding of how temperature affects productivity in nursery habitats, especially in the context of climate change projections. ...
... As thermal regimes become warmer and more variable across the blueback herring range, we can expect changes in adult spawning phenology, zooplankton dynamics and other species interactions to act in antagonistic or synergistic ways with temperature and other habitat factors to affect juvenile physiology (Brodersen et al., 2011;Legett et al., 2021;Lombardo et al., 2019). Thus, it could be beneficial to further investigate and incorporate the impacts of temperature and other ecological factors into management of blueback herring populations in order to improve the efficacy of recovery efforts of this species, thereby benefitting aquatic ecosystems that depend on plentiful, energy-rich prey items (Dias et al., 2019;Walters et al., 2009). ...
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For young fishes, growth of somatic tissues and energy reserves are critical steps for survival and progressing to subsequent life stages. When thermal regimes become supraoptimal, routine metabolic rates increase and leave less energy for young fish to maintain fitness-based activities and, in the case of anadromous fishes, less energy to prepare for emigration to coastal habitats. Thus, understanding how energy allocation strategies are affected by thermal regimes in young anadromous fish will help to inform climate-ready management of vulnerable species and their habitat. Blueback herring (Alosa aestivalis) are an anadromous fish species that remain at historically low population levels and are undergoing southern edge-range contraction, possibly due to climate change. We examined the effects of temperature (21°C, 24°C, 27°C, 30°C, 33°C) on survival, growth rate and energy reserves of juveniles collected from the mid-geographic range of the species. We identified a strong negative relationship between temperature and growth rate, resulting in smaller juveniles at high temperatures. We observed reduced survival at both 21°C and 33°C, increased fat and lean mass-at-length at high temperatures, but no difference in energy density. Juveniles were both smaller and contained greater scaled energy reserves at higher temperatures, indicating growth in length is more sensitive to temperature than growth of energy reserves. Currently, mid-geographic range juvenile blueback herring populations may be well suited for local thermal regimes, but continued warming could decrease survival and growth rates. Blueback herring populations may benefit from mitigation actions that maximize juvenile energy resources by increasing the availability of cold refugia and food-rich habitats, as well as reducing other stressors such as hypoxic zones.
... The most common hake species in tern diets is likely white hake (Kress et al. 2016); however, juveniles are notoriously difficult to identify and may be confused with other similar species such as four-bearded rockling (Enchelyopus cimbrius) or offshore hake (Merluccius albidus). Atlantic Herring (Clupea harengus) likely comprise much of the "herring" category in this study, as they are the numerically dominant Clupeidae in the GoM (Dias et al. 2019); however two species of river herring, alewife (Alosa pseudoharengus) and blueback herring (Alosa aestivalis), may also occur in chick diets. Two species of sand lance occur in the GoM and are indistinguishable based on visual observations alone. ...
... For example, through restoration of western Atlantic River herring (Alosids spp), there is potential to benefit the entire marine food web by reducing pressures on other forage fishes and relaxing pressures among competing consumers (Dias et al., 2019). In tropical rivers, seasonal migrations of herbivorous fishes' link eutrophic and oligotrophic systems, causing shifts in food web structure and potentially subsidizing predators (Winemiller & Jepsen, 1998). ...
Movement of fishes in the aquatic realm is fundamental to their ecology and survival. Movement can be driven by a variety of biological, physiological, and environmental factors occurring across all spatial and temporal scales. The intrinsic capacity of movement to impact fish individually (e.g., foraging) with potential knock‐on effects throughout the ecosystem (e.g., food web dynamics) has garnered considerable interest in the field of movement ecology. The advancement of technology in recent decades, in combination with ever‐growing threats to freshwater and marine systems, have further spurred empirical research and theoretical considerations. Given the rapid expansion within the field of movement ecology and its significant role in informing management and conservation efforts, a contemporary and multidisciplinary review about the various components influencing movement is outstanding. Using an established conceptual framework for movement ecology as a guide (i.e., Nathan et al., 2008 PNAS. 105:19052), we synthesize the environmental and individual factors that affect the movement of fishes. Specifically, internal (e.g., energy acquisition, endocrinology, and homeostasis) and external (biotic and abiotic) environmental elements are discussed, as well as the different processes that influence individual‐level (or population) decisions, such as navigation cues, motion capacity, propagation characteristics, and group behaviours. In addition to environmental drivers and individual movement factors, we also explore how associated strategies help survival by optimizing physiological and other biological states. Next, we identify how movement ecology is increasingly being incorporated into management and conservation by highlighting the inherent benefits that spatio‐temporal fish behaviour imbues into policy, regulatory, and remediation planning. Finally, we consider the future of movement ecology by evaluating ongoing technological innovations and both the challenges and opportunities that these advancements create for scientists and managers. As aquatic ecosystems continue to face alarming climate (and other human‐driven) issues that impact animal movements, the comprehensive and multidisciplinary assessment of movement ecology will be instrumental in developing plans to guide research and promote sustainability measures for aquatic resources. This article is protected by copyright. All rights reserved.
... Alewife have a long history of economic and cultural importance to regional commercial and recreational fisheries as well as to indigenous cultures as food and bait (Hall et al. 2012;Alexander et al. 2017;Mattocks et al. 2017;Daigle et al. 2019). Alewife serve as important links between lower and upper trophic levels as planktivores as well as key forage to higher-level fishes, marine mammals, and seabirds (Mullen et al. 1986;Moring and Mink 2002;Dias et al. 2019). They provide other important ecosystem services as conduits of marinederived nutrients between freshwater and ocean environments (Durbin et al. 1979). ...
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The timing of biological events in plants and animals, such as migration and reproduction, is shifting due to climate change. Anadromous fishes are particularly susceptible to these shifts as they are subject to strong seasonal cycles when transitioning between marine and freshwater habitats to spawn. We used linear models to determine the extent of phenological shifts in adult Alewife Alosa pseudoharengus as they migrated from ocean to freshwater environments during spring to spawn at 12 sites along the northeastern USA. We also evaluated broadscale oceanic and atmospheric drivers that trigger their movements from offshore to inland habitats, including sea surface temperature, North Atlantic Oscillation index, and Gulf Stream index. Run timing metrics of initiation, median (an indicator of peak run timing), end, and duration were found to vary among sites. Although most sites showed negligible shifts towards earlier timing, statistically significant changes were detected in three systems. Overall, winter sea surface temperature, spring and fall transition dates, and annual run size were the strongest predictors of run initiation and median dates, while a combination of within‐season and seasonal‐lag effects influenced run end and duration timing. Disparate results observed across the 12 spawning runs suggest that regional environmental processes were not consistent drivers of phenology and local environmental and ecological conditions may be more important. Additional years of data to extend time series and monitoring of Alewife timing and movements in nearshore habitats may provide important information about staging behaviors just before adults transition between ocean and freshwater habitats.
... However, energy flow to higher trophic levels within a Gulf of Maine estuary is driven by marine planktivores, such as Atlantic Herring and sand lances Ammodytes spp., rather than juvenile river herring (Figure 9). A recent study concluded that restoration of river herring populations could result in a moderate increase of marine predators, including groundfish, sharks, seabirds, and marine mammals (Dias et al. 2019). ...
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River herring—a collective name for the Alewife Alosa pseudoharengus and Blueback Herring A. aestivalis—play a crucial role in freshwater and marine ecosystems along the Eastern Seaboard of North America. River herring are anadromous and return to freshwater habitats in the tens to hundreds of millions to spawn, supplying food to many species and providing nutrients to freshwater ecosystems. After two and a half centuries of habitat loss, habitat degradation, and overfishing, river herring are at historic lows. In 2013, National Oceanic and Atmospheric Administration Fisheries established the Technical Expert Working Group (TEWG) to synthesize information about river herring and to provide recommendations to advance the science related to their restoration. This paper was composed largely by the chairs of the TEWG subgroups and represents a review of the current state of knowledge of river herring, with an emphasis on identification of threats and discussion of recent research and management actions related to understanding and reducing these threats. Important research needs are then identified and discussed. Finally, current knowledge is synthesized, considering the relative importance of different threats. This synthesis identifies dam removal and increased stream connectivity as critical to river herring restoration. Better understanding and accounting for predation, climate change, and fisheries are also important for restoration. Finally, there is recent evidence that the effects of human development and contamination on habitat quality may be more important threats than previously recognized. Given the range of threats, an ecosystem approach is needed to be successful with river herring restoration. To facilitate this ecosystem approach, collaborative forums such as the TEWG (renamed the Atlantic Coast River Herring Collaborative Forum in 2020) are needed to share and synthesize information among river herring managers, researchers, and community groups from across the species’ range.
... While decision-making at dams involves a wide range of stakeholders with diverse and sometimes conflicting objectives (Roy et al., 2018), "active restoration" has been framed as a balanced approach that integrates both values and science (Hart et al., 2002). There is a growing appreciation for the biological and economic benefits of restoring coastal connectivity (Dias et al., 2019), thereby regaining that which we have lost. ...
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American shad ( Alosa sapidissima ) are native to the east coast of North America from the St. Johns River, Florida, to the St. Lawrence River region in Canada. Since the 1800s, dams have reduced access to spawning habitat. To assess the impact of dams, we estimated the historically accessed spawning habitat in coastal rivers (485,618 river segments with 21,113 current dams) based on (i) width, (ii) distance from seawater, and (iii) slope (to exclude natural barriers to migration) combined with local knowledge. Estimated habitat available prior to dam construction (2,752 km ² ) was 41% greater than current fully accessible habitat (1,639 km ² ). River-specific population models were developed using habitat estimates and latitudinally appropriate life history parameters (e.g., size at age, maturity, iteroparity). Estimated coast-wide annual production potential was 69.1 million spawners compared with a dammed scenario (41.8 million spawners). Even with optimistic fish passage performance assumed for all dams (even if passage is completely absent), the dam-imposed deficit was alleviated by fewer than 3 million spawners. We estimate that in rivers modeled without dams, 98,000 metric tons of marine sourced biomass and nutrients were annually delivered, 60% of which was retained through carcasses, gametes and metabolic waste. Damming is estimated to have reduced this by more than one third. Based on our results, dams represent a significant and acute constraint to the population and, with other human impacts, reduce the fishery potential and ecological services attributed to the species.
... Reducing non-climate stressors can increase the resilience not just of individual species, but also entire ecosystems through improvements in fitness, survival, and the competitive abilities of sensitive species (Floury et al. 2013;Staudt et al. 2013;Lynch et al. 2016). Familiar actions such as increasing habitat connectivity enhance species (e.g., diadromous fishes) ability to recover from long-term depletion and expand ecological roles within food-webs and socio-economic systems (Dias et al. 2019). Increasing connectivity also allows species to adapt to climate impacts and colonize new areas by providing corridors to follow thermal optima (Krosby et al. 2010). ...
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Emergent properties of ecosystems are community attributes, such as structure and function, that arise from connections and interactions (e.g., predator–prey, competition) among populations, species, or assemblages that, when viewed together, provide a holistic representation that is more than the sum of its individual parts. Climate change is altering emergent properties of aquatic ecosystems through component responses, a combination of shifts in species range, phenology, distribution, and productivity, which lead to novel ecosystems that have no historical analog. The reshuffling, restructuring, and rewiring of aquatic ecosystems due to climate impacts are of high concern for natural resource management and conservation as these changes can lead to species extinctions and reductions in ecosystem services. Overall, we found that substantial progress has been made to advance our understanding of how climate change is affecting emergent properties of aquatic ecosystems. However, responses are incredibly complex, and high uncertainty remains for how systems will reorganize and function over the coming decades. This cross‐system perspective summarizes the state of knowledge of climate‐driven emergent properties in aquatic habitats with case studies that highlight mechanisms of change, observed or anticipated outcomes, as well as insights into confounding non‐climate effects, research tools, and management approaches to advance the field.
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The timing of life history events in many plants and animals depends on the seasonal fluctuations of specific environmental conditions. Climate change is altering environmental regimes and disrupting natural cycles and patterns across communities. Anadromous fishes that migrate between marine and freshwater habitats to spawn are particularly sensitive to shifting environmental conditions and thus are vulnerable to the effects of climate change. However, for many anadromous fish species the specific environmental mechanisms driving migration and spawning patterns are not well understood. In this study, we investigated the upstream spawning migrations of river herring Alosa spp. in 12 coastal Massachusetts streams. By analyzing long‐term data sets (8–28 years) of daily fish counts, we determined the local influence of environmental factors on daily migration patterns and compared seasonal run dynamics and environmental regimes among streams. Our results suggest that water temperature was the most consistent predictor of both daily river herring presence–absence and abundance during migration. We found inconsistent effects of streamflow and lunar phase, likely due to the anthropogenic manipulation of flow and connectivity in different systems. Geographic patterns in run dynamics and thermal regimes suggest that the more northerly runs in this region are relatively vulnerable to climate change due to migration occurring later in the spring season, at warmer water temperatures that approach thermal maxima, and during a narrower temporal window compared to southern runs. The phenology of river herring and their reliance on seasonal temperature patterns indicate that populations of these species may benefit from management practices that reduce within‐stream anthropogenic water temperature manipulations and maintain coolwater thermal refugia.
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Aging infrastructure and growing interests in river restoration have led to a substantial rise in dam removals in the United States. However, the decision to remove a dam involves many complex trade-offs. The benefits of dam removal for hazard reduction and ecological restoration are potentially offset by the loss of hydroelectricity production, water supply, and other important services. We use a multiobjective approach to examine a wide array of trade-offs and synergies involved with strategic dam removal at three spatial scales in New England. We find that increasing the scale of decision-making improves the efficiency of trade-offs among ecosystem services, river safety, and economic costs resulting from dam removal, but this may lead to heterogeneous and less equitable local-scale outcomes. Our model may help facilitate multilateral funding, policy, and stakeholder agreements by analyzing the trade-offs of coordinated dam decisions, including net benefit alternatives to dam removal, at scales that satisfy these agreements.
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Migrating adult Alewives Alosa pseudoharengus are a source of marine‐derived nutrients on the East Coast of North America, importing nitrogen and phosphorus into freshwater habitats. Juvenile migrants subsequently transport freshwater‐derived nutrients into the ocean. We developed a deterministic model to explore the theoretical nutrient dynamics of Alewife migrations at differing spawner abundances. Net nutrient balance was calculated relative to these abundances along the spawner–recruit curve. The ecological consequences of these subsidies in a particular watershed depend on the magnitude of adult escapement relative to the habitat's carrying capacity for juveniles. At low escapement levels and assuming complete habitat access, the number of recruits produced per spawner was high and juvenile nutrient export dominated. At high escapement levels, fewer recruits were produced per spawner because recruitment is density dependent. As a result, adult nutrient import dominated. At varying levels of freshwater productivity and fisheries mortality for upstream spawners, this trend remained the same while the magnitude of the endpoints changed. Productivity level was the major determinant of export, while fisheries mortality had the strongest effect on adult import. The dynamics of this nutrient trade‐off are important for managers to consider as a recovering population will likely shift from net export to net import as escapement increases. This transition will be sensitive to both harvest rates and to fish passage efficacy at dams and other barriers.
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Atlantic cod (Gadus morhua) in the Gulf of Maine (GOM) is an iconic marine fishery stock that has experienced a substantial distributional shift since the mid-1990s. A geostatistical delta-generalized linear mixed model was utilized to hindcast yearly season-specific distributions of GOM cod. These distributions were calculated using the spring and fall bottom trawl survey data for the stock, along with cell-based bathymetry and bottom temperature data for the study area for the years 1982-2013. The centre of stock distribution (the centre of gravity), spatial extent in latitude and longitude, area occupied and median habitat temperature were estimated annually to quantify changes in the spatial dynamics of GOM cod. Time series of these distributional metrics were then used to evaluate the influences of climate change and densitydependent habitat selection on GOM cod's distribution. Results showed that the rapid southwestward shift in the stock distribution after the late 1990s could not simply be attributed to decreasing stock abundance or warming bottom temperatures. The observed shift in cod distribution requires further investigation on whether it is possibly a result of other factors, like fluctuating productivity among subpopulations. © 2017 International Council for the Exploration of the Sea. All rights reserved.
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Asymmetries in responses to climate change have the potential to alter important predator-prey interactions, in part by altering the location and size of spatial refugia for prey. We evaluated the effect of ocean warming on interactions between four important piscivores and four of their prey in the U.S. Northeast Shelf by examining species overlap under historical conditions (1968-2014) and with a doubling in CO2. Because both predator and prey shift their distributions in response to changing ocean conditions, the net impact of warming or cooling on predator-prey interactions was not determined a priori from the range extent of either predator or prey alone. For Atlantic cod, an historically dominant piscivore in the region, we found that both historical and future warming led to a decline in the proportion of prey species’ range it occupied and caused a potential reduction in its ability to exert top-down control on these prey. In contrast, the potential for overlap of spiny dogfish with prey species was enhanced by warming, expanding their importance as predators in this system. In sum, the decline in the ecological role for cod that began with overfishing in this ecosystem will likely be exacerbated by warming, but this loss may be counteracted by the rise in dominance of other piscivores with contrasting thermal preferences. Functional diversity in thermal affinity within the piscivore guild may therefore buffer against the impact of warming on marine ecosystems, suggesting a novel mechanism by which diversity confers resilience. This article is protected by copyright. All rights reserved.
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This paper explores the impact of fishing low trophic level “forage” species on higher trophic level marine predators including other fish, birds and marine mammals. We show that existing analyses using trophic models have generally ignored a number of important factors including (1) the high level of natural variability of forage fish, (2) the weak relationship between forage fish spawning stock size and recruitment and the role of environmental productivity regimes, (3) the size distribution of forage fish, their predators and subsequent size selective predation (4) the changes in spatial distribution of the forage fish as it influences the reproductive success of predators. We show that taking account of these factors generally tends to make the impact of fishing forage fish on their predators less than estimated from trophic models. We also explore the empirical relationship between forage fish abundance and predator abundance for a range of U.S. fisheries and show that there is little evidence for a strong connection between forage fish abundance and the rate of change in the abundance of their predators. We suggest that any evaluation of harvest policies for forage fish needs to include these issues, and that models tailored for individual species and ecosystems are needed to guide fisheries management policy.
Recent research has demonstrated the important role that high-biomass species play in the transfer of energy and nutrients across habitat boundaries, as well as the ecosystem consequences of their loss. To contrast the historical and current biomass of historically abundant anadromous forage fish, we combined historical records of habitat loss from damming with contemporary freshwater productivity of alewives and diet data of freshwater predator fish. Significant declines in production occurred by 1850 in the northeastern United States, long before any direct abundance data were available, which would have had significant effects on freshwater prey resources for the numerous predators directly affected by the transfer of nutrients across the freshwater–marine nexus. Current freshwater systems operate at approximately 6.7% of historical capacity of anadromous alewife biomass and abundance. This provides an example of habitat-mediated changes in connectivity limiting nutrient flux and energy flow among populations and species that alter ecosystem function at multiple scales.
Resource pulses provide consumers with opportunities to feed at high rates. The spawning and die-off of semelparous Pacific salmon provide consumers with feeding opportunities that contribute substantially to annual energy budgets. The life history of Pacific salmon also includes the downstream migration of smolts, which could provide similar opportunities for consumers to exploit. We tracked seasonal movements of adult Bull Trout Salvelinus confluentus in and out of the Chilko Lake-River outlet in interior British Columbia, which is character- ized by a large Sockeye Salmon Oncorhynchus nerka population. Use of the outlet, lake, and river habitats were compared with the timing of out-migrations of Sockeye Salmon smolt and the spawning events of Sockeye Salmon, Chinook Salmon O. tshawytscha, and Coho Salmon O. kisutch. Bull Trout activity and residency in the outlet increased during the spring Sockeye Salmon smolt out-migration, and 40% of Bull Trout were found to return to the outlet in successive years. During Sockeye Salmon spawning, Bull Trout residency was increased in the river where most Sockeye Salmon spawning occurs. Therefore, Bull Trout may exploit both life history events, although direct consumption of eggs was not observed. Spawning by Chinook Salmon and Coho Salmon in the river did not appear to attract Bull Trout; Bull Trout residency increased in the lake (where spawning does not occur) during these times. Bull Trout residency in the lake also increased when outlet water temperatures were >16°C, and thus the lake may provide thermal refuge when river temperatures are above optima for this coldwater char. This research demonstrates that movements of aquatic consumers can depend upon smolt out-migrations, and such movements can allow exploitation of multiple pulses that are seasonally distinct. These results also highlight the ecological significance of Pacific salmon for consumers in freshwater systems.