Outline of INVASAL White paper

Title: The need for a comprehensive assessment of salmonid invasionseof non-native salmonids in a
large region of South America with high faunistic endemicity

Authors’ list (proposal): Gomez-Uchida D, TA Contador, B Ernst, M Sepúlveda, S Neira, B Cid-Aguayo,

CB Canales-Aguirre, P Bahamonde, C Quezada-Romegialli, A Ramírez, JM Yáñez, LW Seeb, JE Seeb, I
Vila, TP Quinn, DE Schindler, BJ Hicks & C Harrod

Target journal: BioScience (IF: 4.7). Máx 5,000 words excluding refs, tables, figs,

Abstract

Strong latitudinal and altitudinal gradients and extreme ranges of climatic conditions found in the western
region of South America where Chile is located characterize the habitats of several species of invasive
salmonids. They were successfully introduced to both marine and freshwater systems for over a century
and now live in sympatry with a highly endemic biota distributed along nearly 4,000 km of territory. The
presence of non-native salmonids has dramatically altered economic and social landscapes of this region
amid scattered efforts to for quantifying their ecological impacts on native ecosystems. We found
important knowledge gaps on (1) species distribution, (2) ecological interactions with native taxa, and (3)
societal importance and uses, including recreational and commercial opportunities, which are likely to
influence decisions regarding control, suppression, and eradication of salmonids. We argue provide
examples arguing that management of salmonid invasions needs be case-specific and goals demand a
comprehensive assessment of ecological and socioeconomic impacts to achieve desired changes in
policy. Such assessment needs to hinge on a network of scientists from diverse scientific backgrounds in
order to achieve desired changes in policy and management of these invasive, yet valuable species.

Keywords: Salmonidae, fisheries, aquaculture, management, invasive species, social science

The isolated and highly endemic south western region of South America

Continental Chile represents a microcosm of much of the globe: located in the south-western extreme of
South America, it extends from the tropics to the sub-Antarctic, and marked latitudinal and altitudinal
gradients result in extreme ranges of climate conditions. Extreme latitudinal range of bioclimatic types…
(Fig. 1)

Hotspot of biodiversity… endemic fishes… invertebrates…

How invasions of non-native salmonids have changed native ecosystems

Human-mediated introductions of non-native species have profound consequences on native receiving

ecosystems. Invasive species may cause community changes and population declines among native
species, leading to loss of ecosystem services. they may also ecologically interact with multiple species
and have far reaching community consequences, acting as predators, prey, or both, as well as
competitors and sources of pathogens and parasites. Disentangling these roles is crucial to developing
both the efficient management of invasive species and effective conservation strategies for native
species. Today, populations of non-native salmonids are found in almost every catchment from the
northern border with Peru to Cape HornNavarino Island in the south.
Salmonids are important subjects in ecology and evolution in their native range. They show significant
variation in life histories, including semelparous (one reproductive event) vs. iteroparous reproduction
(multiple reproductive events), anadromous (migrate to sea to feed but return to breed in freshwater) vs.
resident forms (entire life cycle in freshwater), and yearly vs. sub-yearly residence of juveniles in
freshwater before migrating to sea. They also home to their natal streams with extraordinary precision to
breed, which permits the evolution of reproductive isolation and local adaptation between populations at
various scales, ranging from tributaries to watersheds. Salmonids can be also considered keystone
species especially in relation to breeding. Nest digging by female salmon to deposit their eggs results in
significant amounts of bioturbation and disturbance of the riverbed, fundamentally affecting nutrient
cycling and ecosystem metabolism. Carcasses from semelparous salmonids generate large amounts of
marine-derived elements available for consumption and recycling by resident taxa, and elements are
often transferred from the river channel to riparian areas by floods and by predators and scavengers.
Marine-derived nutrients supplied by decomposing salmon may play important roles fertilizing receiving
ecosystems in North America, Japan and Europe. The connections between breeding salmonids and
other taxa suggest positive feedback mechanisms, species coevolution, and complex ecosystem
networks of energy transfer that are yet to be tested elsewhere.

The introduction of salmonids (family Salmonidae) to Chile in South America is an exemplary case of a
complex invasion with both perceived negative and positive impacts, making the presence of salmonids in
Chile a controversial topic. Salmonids were repeatedly introduced as a result of both aggressive
government- and privately-funded initiatives implemented since the start of the twentieth century. These
included stocking of lakes and river systems to promote recreational and commercial fisheries (1900 -
1990) and the promotion and rapid development of salmonid aquaculture (1980 - present), both in
freshwater and marine coastal areas. At least five species of salmonids from the Pacific (genus
Oncorhynchus) and Atlantic lineages (genus Salmo) have established and spread in Chile and South
America (Table 1). Salmon and trout aquaculture have positioned Chile as the world’s second largest
salmon producer, but at high environmental costs: habitat degradation, possible links to algal blooms, and
impacts of salmonid escapes from aquaculture facilities.

How non-native salmonids have changed social and economic landscapes and the need for a
comprehensive assessment

Biological invasions are also complex phenomena with ecological, evolutionary, environmental, and social
dimensions, often providing mixed impacts. Invasive species can be economically important, priming the
development of emerging economies. Thus speaking of invasive species places us at the interface
between nature and culture, power-work-discourse and ecological dynamics: the field of political ecology.
This field has gone from perspectives that assume the social and the environmental as separate realities,
towards relational points of view. The former, with Malthusian inspiration, understood the environment as
an external limit to socioeconomic growth. The second ones involve materialist and constructivist
positions, focus on the economic and political production of nature as well as its socio-material and
linguistic construction.
Lefebvre (2013) and Smith (1990 )describe how first nature suffers a historical processes of appropriation
and modification, through production and work, producing a second nature. This involves a transformation
of the way nature is produced and reproduced: socially produced, but not totally controlled by work and
science The metabolism of this produced nature, conserves and generates its distinctive ecology, then
the nature-social contradiction becomes an irreducible property of the socio-natural network. From a
constructivist vision, the interdependence between the social and the natural is expressed in the language
of symmetry and co-construction. Latour (2006) proposes symmetric descriptions of how human and non-
human actors -nature, and technology- interact, form heterogeneous networks that act collectively and
form our world. Invasive species would be clear examples of quasi-objects Latourinans (of social and
natural origin), the product of human intervention, and creating a distinctive ecology that transcends social
control and has unanticipated effects. These approaches break a binary thought: If the domination of
nature is an inevitable aspect of social life, the only alternatives are an antisocial politics of nature or seek
a less harmful domination. Ontological vision of a supposedly prehuman nature invisibilizes the processes
of human work and science (SMITH, 1990). Latour (2004), advocates transcending such binarism to
account for the social construction of facts and nature recognizing the autonomy of natural world
processes. In other words, as Pollan (1991) affirms, to really assume the idea of "second nature" opens
the ethical questions on how to use and even modify nature without damaging its reproductive condition;
that is metaphorically how to "cultivate" in a way that nature and culture benefit.

This involves to"... identify, consider and evaluate changes in various aspects of people's lives, including
their way of life, culture, community, biophysical environment, economic systems and mental, physical,
social and psychological well-being ... "(FITZGERALD AND WILKINSON, 2009, p.6). Llorente and others
(2011) point to the role of local stakeholders in the identification of problems and ways to manage
invasions. This is due to its multifaceted nature where "... From a utilitarian perspective, not all invasive
species are harmful, but they may offer economic benefits (LLORENTE et al, 2011 p.3). Thus the attitude
of the communities "... varies depending on the specific impacts that the species have on their livelihoods,
enjoy the landscape, and their aesthetic sense of the environment, phylogenetic bias, knowledge and
experience with their local ecosystem ..." (FORTWANGLER, 2013, p.5). In such complex cultural contexts
a participatory work approach is needed, capable of "compiling information on the potential
consequences of invasive species on social, economic and cultural values, including the values and
priorities of indigenous people and local communities" ( ADAMS et al, 2018, pp.2). Our view thus
includes, on the one hand, a constructivist vision of nature, where the landscape and nature are actively
produced and signified by humans; which gives us the responsibility of managing a sustainable habitat for
all its members. This process involves the perceptions and actions of various stakeholders, which may be
contradictory. This must also be an approach that includes the multiple tissue of interrelations between
humans and non-humans.

RESUMIR
… (Fig. 1)

The introduction of non-native salmonid fishes to Chile and the world has been a remarkable success -
providing access to jobs, food and recreation to regions with little economic opportunities. Naturalized
salmonids also support recreational fisheries and emerging, small-scale commercial fisheries.
Understanding the impacts of salmonids at various levels of biological organization is necessary to
balance the importance of their presence in Chile’s ecosystems. However, salmonids are also highly
invasive and have extremely adverse impacts on native ecosystems. In Chile, the presence of salmonids
is controversial, and has marked implications for the socioeconomic and ecological wellbeing of the
country and the natural resources on which it depends. There is a pressing need to count with evidence-
based policy for the future management of invasive salmonids in Chile by asking What and where are
the ecological and socioeconomic impacts of invasive salmonids in Chile and how this
information can be used to develop and implement evidence-based management solutions and
(through?) policy?

The mission of the Millennium Nucleus of Invasive Salmonids (INVASAL) is to: (1) undertake world-
class research with national and global impact using cutting-edge techniques to characterize the
distribution and impacts of free-living salmonids on native ecosystems, both in fresh- (lakes rivers and
streams) and coastal-waters, including population-, community- and ecosystem-level effects, and their
societal impacts; (2) understand how Chilean society uses and values free-living salmonids; (3) develop
tools for resource managers, conservation biologists, enforcement personnel and industry and
disseminate findings to them and other stakeholders including fishers, NGOs and society at large, in order
to improve and develop efficient policy and management strategies for both invasive salmonids and
native aquatic communities; and (4) mentor students, professionals, and young researchers in a friendly,
welcoming environment where equality is strived for.

Our proposed activities are organized around four major scientific themes that connect salmonid
population biology, the aquatic ecosystems that free-living salmonids inhabit, and the stakeholders that
interact with salmonids. These are connected by a fifth cross-cutting theme: our mission to become a
world class center in educating students and young investigators and informing stakeholder on the
importance of studying invasions as complex phenomena through the lens of multiple disciplines (Fig. 1).

Theme Knowledge gap #1: Mapping the current distribution of salmonids & native fishes

Given the distribution of salmonid fishes throughout Chile, there is a pressing need for current information
on their status, their actual - not perceived - impacts on receiving habitats, native species, and supporting
ecosystems and their importance to and use by human populations. A combination of field-based
sampling, interviews (e.g., fisheries scientists, anglers, fishing guides, hatchery managers and other
stakeholders), literature reviews and social media monitoring, should yield the most comprehensive data
set to date. These data will be integrated using a geographic information system into a dynamic and open
access map of the distribution of salmonid and native fishes in Chile.

We will use the recently developed environmental DNA (eDNA) approach for rapid assessments of the
presence of native/non-native fishes in rivers across continental Chile. This involves sampling water from
a given habitat, concentrating, extracting and sequencing DNA to identify species present at a site. The
use of eDNA is revolutionizing the assessment of fish distributions and by undertaking national-scale
study…

Theme 2Knowledge gap #2: Evaluating ecological interactions between salmonids & native taxa

The biomass of salmonids in Chilean freshwaters is likely greater than for all native fishes combined,
reflecting their innate plasticity and flexible diet, and competitive superiority over native fishes, which in
freshwater tend to be endemic, small bodied and less aggressive. Salmonids can attain large individual
sizes, consuming increasing amounts of invertebrates and fish as they grow. In marine habitats, Chinook
salmon can gain ca. 10kg a year feeding on small fish and krill. Conversely, despite undergoing predator
release in Chile, invasive salmonids represent an ecological opportunity for piscivorous predators, both
native (e.g. marine mammals, fish eating birds) and introduced (American mink), and predation on
salmonids has been markedly understudied in Chile.

Stomach content analyses suggest that Chinook Salmon can feed largely on small pelagics, and this has
important consequences for ecosystem-based management approaches. Energy subsidies and
ecosystem implications of Chinook Salmon in the coastal ocean and in many watersheds that drain to the
Pacific are currently unknown, and knowledge of how marine-derived nutrients in freshwater introduced
by semelparous salmonids have changed the water-land interphase in upper river systems is lacking. It is
possible that invasive Chinook salmon are facilitating invasions and establishment of non-native Rainbow
Trout, Brown Trout, or both, that capitalize on the marine subsidy provided by spawning fish. In addition to
being a top-level predator, Chinook Salmon have become a significant prey item among marine mammal
populations such as sea lions, suggesting potential positive impacts on mammal populations that need to
be quantified.

Through a common multidisciplinary approach, we will examine ecological interactions between

salmonids and native species including primary producers, putative competitors, prey and predators. We
will characterize the trophic ecology of species and functional groups through an innovative approach,
combining the use of gut contents, stable isotope analysis, gut content DNA-barcoding, and
bioenergetics/food web modeling. We will study this at a series of locations indicative of Chile’s climatic
zones and the diversity of management and ecological challenges associated with salmonid fishes in both
freshwater and marine habitats (Fig. 2). The main output will be a model that synthesizes ecosystem
impacts of non-native salmonids in aquatic environments.

The presence of salmonids potentially influences life history traits of key native fishes and invertebrates
as well as ecosystem functioning.

Theme 3Knowledge gap #3: Understanding the importance of salmonids to Chilean society

Recreational fisheries and farming of non-native salmonids in Chile have been successful, generating
access to jobs, food and recreation (Pascual et al. 2009). However, salmonids are highly invasive with
negative impacts on native ecosystems with associated economic costs (Sepúlveda et al. 2013,
Arismendi et al. 2014, Penaluna et al. 2009). This creates a challenging conservation and management
trade-off between social benefits derived from fishing salmonids and the negative impacts on native
biodiversity.
Chile is globally known for the recreational fisheries targeting naturalized salmonids (Arismendi &
Nahuelhual 2007). However, there is also illegal, unregulated and unreported (IUU) artisanal small-scale
fisheries of salmon populations, e.g. Chinook salmon, providing important economic support to low-
income communities (Musleh 2016). In response to this situation, an emergent governance and
management strategies for these fisheries is being advanced by fisheries authorities and concerned
stakeholders (DS N° 96 2017, FIP 2014-87). In addition, Chile has implemented in 2013 changes in
Fisheries law whose core objectives are the conservation and sustainable use of its living marine
resources. This legislation mandates scientifically based fisheries management using precautionary and
ecosystem approaches (Ley de Pesca y Acuicultura n°20.567, 2013).
This new legislation creates a window of opportunity to guide this emergent governance, towards
implementation of elements of the ecosystem approach to fisheries management, in small-scale fisheries
targeting non-native salmonids
To better meet these challenges, researchers and practitioners focus on understanding linkages between
social and ecological dynamics — often referred to as linked or coupled social-ecological systems (SES)
and how these dynamics affect the fisheries sustainability (Degnbol & Mc Kay 2007). This is part of a
more comprehensive view for the implementation of the ecosystem-based fisheries management
approach (EBFM) (Kittinger et al. 2013).
Emerging governance towards ecosystem-based management in non-native salmonid fisheries requires
an integrated and participatory social-ecological approach to develop implementation frameworks and
management strategies (figure ) (Pascual et al. 2009, Fulton et al. 2014, Folke et al.2016). The Millenium
Nucleus for Invasive salmonids INVASAL (http://www.invasal.cl/) aims to close critical gaps in knowledge
and methodological approaches to implement the ecosystem-based management in non-native salmonid
fisheries: i) analyse the structure and dynamics of the social-ecological systems (SES) involved in the
small scale fisheries targeting non –native salmonids in Chile; ii) reveal components and processes
relevant to the social-ecological fit of emerging governance and management; and iii) understand the
potential sustainability outcomes of emerging governance and management strategies in the small-scale
salmonids fisheries. To achieve this, we will implement a participatory social-ecological system analysis
framework (figure ), involving key stakeholders in order to develop SES models, build desired governance
regime scenarios and test management strategies derived from those scenarios. (Fulton et al. 2015, Ortiz
and Levins 2011; Walker et al. 2006). From a stakeholder viewpoint, this approach focus on a
participative process of building a shared understanding, of the elements that generate and modify the
capacity of a fisheries social-ecological system, to deliver environmental benefits (catch, recreation,
traditions, etc) contributing to desired levels of social wellbeing (Walker et al. 2002, Hillborn et al. 2015,
Fletcher et al. 2014).
Chile is globally famous for the quality of its recreational fisheries targeting naturalized salmonids.
However, there is also large small-scale exploitation of abundant anadromous salmon populations, e.g.
Chinook salmon. Although undocumented, tThey provide major economic support to low-income
communities via the black market. For conservation and management policies to succeed, different
stakeholder values must be considered as salmonid fishes mean different things to different stakeholders.
Salmonids represent an essential source of income to some; to others, they are a form of biological
contamination to be removed to protect native species and ecosystems.

Using interviews and regional workshop-based discussions, we will assess public and stakeholder opinion
on the value of salmonid and native fishes, how the respondents make use of salmonids (or not); their
understanding of conservation issues associated with salmonids, and their estimation of the value of
control measures. Stakeholders will include the public, NGOs, local/national government, conservation
agencies, recreational angling guides/companies, and anglers via various media. We will combine and
present the information generated by Themes 1 and 2 at a series of regional workshops with key
stakeholders. These workshops will guide the production of a key output - an evidence-based policy
document for invasive salmonids in Chile targeted at national and local government, and other
stakeholder groups.

The Lake and Aysén Districts of Chile support the bulk of national aquaculture activity. Aquaculture is key
economic concern in Chile, providing >70% of export income from the south of Chile and employment to
many people. It continues to expand into new locations, representing a major source of potentially
invasive fish wherever fish are cultured. Three commercially important salmonid species unintentionally
escape from aquaculture facilities: Atlantic salmon, coho salmon and rainbow trout. INVASAL researchers
showed that naturalized rainbow trout were genetically divergent from cultured fish. Cultured and
naturalized salmonids are isotopically distinct too, and we will develop genetic-isotopic tools to identify
whether fish are cultured, naturalized or escapees from aquaculture. This will be important to fully
understand the relative ecological impacts of invasive salmonids on marine ecosystems associated with
naturalized and recent escapees.

Given the scale of the potential resource, and the existence of unregulated fisheries for naturalized and
aquaculture-escaped salmon, there is a large potential market for unofficial salmonid products, likely sold
under the label of Atlantic salmon (the most farmed species in Chile). We will examine the use of
naturalized and escapee salmonids in the human food chain after identifying tissues to species by DNA
barcoding and origin (farmed vs. free-living) by stable isotope analysis.

INVASAL will also continue providing estimates of abundance of returning Chinook salmon by using field-
methods to measure abundance (hydroacoustics, spawner and redd surveys) and catch data provided by
stakeholders. These data will allow us to characterize the scale and location of the problem.

Theme 4: Developing methods & policies for the management & control of invasive salmonids
Controlling invasive species is difficult, but some INVASAL workers have led successful efforts to remove
invasive species to conserve native species. We will undertake an effort to remove rainbow trout from the
Chungará system in northern Chile. Lake Chungará, one of the most important freshwater ecosystems in
the Chilean Altiplano, supports a single native species, the endemic Orestias chungarensis. However,
rainbow trout were illegally introduced during the mid-20th century and potentially compete with, and prey
on O. chungarensis.

We will estimate the population size of the rainbow trout population using a series of methods in the lake
and inlet river, providing an indication of the number of fish to be removed. Adult rainbow trout spawn in
the inlet Chungara River and will be trapped and removed during their spawning migration through a
single fixed point. Juvenile fish will be removed after being trapped and electrofished. Visual surveys will
be used to identify and destroy eggs buried in the river bed. We will continue monitoring trout abundance
throughout the project and feel that it is feasible that in a 3-year programme that a major rainbow trout
population can be reduced to a point where it is no longer self-sustaining. This flagship program act as a
case study and provide guidance for similar activities in Chile and worldwide.

Theme 5: Education and outreach

This cross-cutting theme joins the four data-driven themes. The INVASAL team incorporates professional
educators and scientists strongly involved in education and outreach across four continents, and the
project will inform and train the next generation of scientists and citizens. Students and early career
scientists will undertake practical training in the various laboratories in Chile and in our partner
organizations in the US and NZ and annual summer schools. We will inform the next generation of
scientists about the issues associated with INVASAL through school visits and field-schools organized
across the different regions by the excellent CONICYT PAR-EXPLORA scheme.

Several members of the INVASAL team have strong social media presences both in Chile and
internationally. We will maximize publicity and interactions with the public through a dedicated web page
linked to social media accounts detailing the issues behind INVASAL, our activities and production of key
milestones. We will strengthen existing relationships with the traditional media across the regions of Chile,
allowing wide geographical dissemination and the decentralization of science news, which in Chile, is
typically Santiago-centered, unlike the issue of invasive species.

References
Table 1. Most important non-native salmonids introduced to South America and perceived relative ecological and socioeconomic importance.

Species Latitudinal Abundance Aquaculture Fishing References*

distribution
Chinook salmon ++++ +++ + +++ 2,4,5,7,8,9,10,11
O. tshawytscha Imperial River
(Pacific Ocean) to
(Santa Cruz River
Atlantic Ocean ++
+
Rainbow trout
++++ ++++ +++ ++++ 1,2,3,7,8,9,10
O. mykiss
Coho salmon ++ ++ ++ ++ 1,2,8,9,10
O. kisutch
Cherry salmon
O. masou
Atlantic salmon +o + ++++ + 1,2,8,9,10
S. salar
Brown trout +++ +++ o +++ 2,6,7,8,9,10
S. trutta
Brook charr + ++ o ++
S. fontinalis
References: 1.(Arismendi and Nahuelhual 2007); 2(Arismendi et al. 2009); 3(Arismendi et al. 2011); 4(Astorga et al. 2008); 5(Correa and Gross
2008); 6(Faundez et al. 1997); 7(Habit et al. 2010); 8(Niklitschek and Toledo 2011); 9(Soto et al. 2001); 10(Soto et al. 2006); 11(Soto et al. 2007).
Figure 1. Summary of ecological and social settings relevant to study impacts of the presence of invasive salmonids on ecosystems and society.
Figure 2. Social-ecological system analysis framework.