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ICES Journal of Marine Science, 56: 405–409. 1999
Article No. jmsc.1999.0483, available online at http://www.idealibrary.com on
Extinction considerations for diadromous fishes
B. Jonsson, R. S. Waples, and K. D. Friedland
Jonsson, B., Waples, R. S., and Friedland, K. 1999. Extinction considerations for
diadromous fishes. – ICES Journal of Marine Science, 56: 405–409.
Among diadromous fishes, the sturgeons are particularly threatened with 13 of 15
species considered endangered or vulnerable to extinction worldwide. These species
have low intrinsic rate of growth and specialized habitat requirements making them
sensitive to environmental changes and human exploitation. Habitat destruction,
degradation, and alternations are probably prime causes of extinction in diadromous
fishes. The spread of alien species, naturally or transported by humans to new
environments, may be the second most important cause. Harvest is a contributing
factor to extinction risk for many diadromous populations, although there is no
known example where overfishing has led directly to the extinction of species.
Population viability analysis is a method which may be used for evaluating extinction
risk. However, uncertainties associated with parameter estimation and model choice
limit its usefulness. Avoiding short-term extinctions is difficult enough, but restoration
and recovery of natural populations present a whole new array of challenges. The
understanding of the genetic population structure of the species is essential in this
context. Captive rearing has some use as tool to assist stock restoration. However,
artificial propagation will not lead to recovery unless the fundamental problems that
caused the population declines are addressed.
1999 International Council for the Exploration of the Sea
Key words: measuring extinction, population threats, causes of extinction, risk
assessment, habitat restoration, population recovery.
Received 27 March 1998; accepted 16 February 1999.
B. Jonsson: Norwegian Institute for Nature Management, Dronningens gt 13, PO Box
736 Sentrum, N-0105 Oslo, Norway. R. Waples: Conservation Biology Division,
Northwest Fisheries Science Center, 2725 Montlake Boulevard East, Seattle, WA 98112,
USA. K. Friedland: Population Dynamics Branch, Northeast Fisheries Science Center,
166 Water Street, Woods Hole, MA 02543, USA. Correspondence to B. Jonsson: tel:
+47 2335 5000; fax: +47 2335 5101; e-mail: [email protected]
Introduction
Extinction is a natural and inevitable biological process:
the fossil record provides ample evidence that episodes
of unusually high extinction rates occurred in this planet’s past and that species persist for finite periods of
time. In comparison, documented recent extinctions
involve just a small fraction of known animal and
plant species (Smith et al., 1993). Nevertheless, there
is growing concern regarding the fate of Earth’s biodiversity for two reasons: the number of recorded extinctions has climbed steeply over the past century and
growing evidence for human impacts on ecosystems
suggests that the extinction rate may increase rapidly in
the future.
The collection of papers in this issue examine various
aspects of extinction risk for diadromous fishes, which
by definition must migrate between fresh water and salt
1054–3139/99/040405+05 $30.00/0
water (or vice versa) to complete their life cycle
(McDowall, 1999). These papers were part of a special
theme session entitled ‘‘Diadromous Fish Extinction:
Threats on Local and Global Scales’’ at the annual ICES
Science Meeting held in Baltimore, Maryland (USA) in
September 1997.
Measuring extinction
In exceptional cases, the last few members of a species
can be monitored closely, and an extinction is recorded
when the last individual dies. In general, however,
measuring extinction is not a straightforward process.
Both absolute and relative estimates of extinction rates
are subject to a number of biases related to sampling
effort, detectability, taxonomic uncertainty, and inadequate understanding of the organism’s biology (Smith
1999 International Council for the Exploration of the Sea
406
B. Jonsson et al.
et al., 1993). A common practice (used, for example, by
the World Conservation Monitoring Centre) is to consider a species extinct if it has not been observed for 50
years. This method may be reliable for once common
and frequently encountered species, but it will be less so
for species that have always been cryptic, seclusive, or
otherwise difficult to observe. Grogan and Boreman
(1999) showed how to calculate the probability that
diadromous fish species have been extirpated, using a
method that takes into account the temporal pattern of
historic observations of the species. They also pointed
out that in evaluating extinction probability for fish
species, special care is needed if historical observations
of early life stages are used, since fluctuations in abundance over time there are generally much larger than for
the adult phase.
Threats to diadromous fishes
Due to their migratory habits, diadromous fishes may be
at generally higher risk of extinction than many other
groups and present special conservation challenges.
Whereas approximately 5% of all fish species are
considered endangered, threatened, vulnerable, rare, or
of indeterminate status (Barbault and Sastrapradja,
1995), McDowall (1999) has identified about 18% of
diadromous species that are of some conservation
concern. One group, the sturgeons (Acipenser spp.),
are particularly imperilled, both in Europe and Asia.
This concerns both anadromous and freshwater resident
populations. According to the IUCN Red List of
Threatened Animals (Baillie and Groombridge,
1996), one species is critically endangered, facing an
extremely high risk of extinction in the wild in the
immediate future; eight other species are endangered
and four species are vulnerable. Only two of the 15
anadromous sturgeons are low-risk species. The sturgeons are particularly vulnerable because they are
long-lived with low intrinsic rates of population growth
and their specialized spawning requirements make them
sensitive to environmental changes as well as human
exploitation.
Other taxa of particular concern include the
Prototroctidae (southern graylings) and the Alosinae
(shads) (McDowall, 1999). Of the two southern grayling
species, one is extinct and the other threatened. Reasons
for their decline are probably combined effects of deforestation and trout introductions (McDowall, 1990).
One shad in the Gulf of Mexico is endangered, and
the two shads in the East Atlantic are vulnerable.
For anadromous salmonids entire species appear
not to be in any immediate danger of extinction, but
many local spawning populations have been extirpated,
and many more face significant risk of extinction
(Kellogg, 1999).
Causes of extinction
Although human impacts have greatly increased species
risks over the past century, extinctions rarely are due to
one factor alone but instead involve the interplay of
anthropogenic effects, natural factors, chance events,
and biological attributes of the species. Threatened
species are often characterized by one or more of the
following: large body size, high trophic level, small
population size, restricted geographic distribution, poor
dispersal and colonizing abilities, colonial breeding habits, dependence on specialized habitats or ecosystems,
migratory life history, dependence on unreliable
resources, and inability to respond to environmental
change or disturbances (Reid and Miller, 1989).
Some of these risk factors apply to diadromous
species, all of which are migratory and many of which
are relatively large and near the top of the food web.
Most diadromous species are widely distributed, but
local populations typically occupy restricted areas and
may be strongly isolated. Spawning populations range
from relatively small (as is usually the case for Atlantic
salmon, Salmo salar) to quite large units [as in many
populations of pink salmon (Oncorhynchus gorbuscha)
and sockeye salmon (O. nerka) in the Pacific].
Probably the most pervasive anthropogenic influence
on extinction risk for diadromous fishes has been
destruction, degradation, or alteration of habitat
(Nehlsen et al., 1991; McDowall, 1999; Lichatowich
et al., 1999; McKinnell and Karlström, 1999). Destruction and modification of habitat occurs through a wide
variety of human activities, including forestry, agriculture, ranching, mining, hydropower development, and
urbanization. Effects range from short term, localized
modifications of habitat structure and function to alteration of ecosystem processes and structure (Gregory and
Bisson, 1997). For example, the Atlantic salmon populations in southern Norway have been lost due to
acidification of the freshwater habitats (Hesthagen and
Hansen, 1991), and more than 90% of the Baltic salmon
populations have been lost due to river regulation for
hydropower purposes (Ackefors et al., 1991).
Although we are not aware of any case in which
overfishing has led directly to species extinction, harvest
is a contributing factor to extinction risk for many
populations of diadromous fishes. The predominant
paradigm in harvest management for salmon has been
based on taking a fixed percentage of the population.
Cass and Riddell (1999) used a stochastic life cycle
model to evaluate the interplay of harvest and natural
variability in abundance for some British Columbia
populations of chinook salmon (O. tshawytscha). Their
results indicate that current fixed-rate harvest policies
are not risk averse, nor are they likely to result in
maximum long-term economic benefits. An alternative
strategy which includes a minimum escapement floor
Extinction considerations for diadromous fishes
before any harvest is allowed provides much greater
protection from extinction and greater long-term economic benefits than the current strategy. A modification
of the threshold strategy to allow harvet rates to increase
with increasing stock biomass could help alleviate some
of the concerns for the economic and social effects of
prohibiting all harvests in years of low abundance.
Another cause of extinction is interaction with alien
species, spread naturally or, more frequently, transported by humans to new environments. Some introductions are relatively benign, but others cause major
disruptions to ecosystems and may play a significant role
in elevating extinction risk. The spread of nonindigenous species is second only to habitat destruction
in harming native communities and causing population
extinction (Barbault and Sastrapradja, 1995). Humans
have also enhanced the spread of diseases and parasites,
which may be more responsible for population declines
than is commonly recognized (McCallum and Dobson,
1995). For example, the monogenous parasite Gyrodactylus salaris was first introduced into a Norwegian river
in the mid 1970s, and by 1991 it could be found in 35
rivers. This parasite causes a catastrophic mortality of
Atlantic salmon parr; typically, parr are nearly absent
from a river 2 years after Gyrodactylus is first observed
(Heggberget et al., 1993). It has been estimated that
Gyrodactylus may be responsible for a 50% reduction in
the natural production of salmon in Norway (Johnsen
and Jensen, 1991).
A swimbladder parasite of the Japanese eel, Anguillicola crassus, was introduced to Europe together with
living European eels, Anguilla anguilla, at the beginning
of the 1980s. Within 10 years of its introduction it had
achieved high rates of infection intensities in populations
of the European eel over most of Europe (Hartmann,
1994). This parasite destroys the swimbladder of the
host, with the likely consequence that eels with nonfunctional swimbladders will fail to reach their breeding
grounds. The recent discovery of its appearance in
American eels, Anguilla rostrata, in South Texas and
South Carolina (Fries et al., 1996), is further reason for
concern.
Estimating extinction risk
Key to avoiding extinction of a species is to detect which
species are particularly sensitive. Evaluating extinction
risk involves estimating the probability that a species (or
population) will not persist for a given length of time. In
the past 15 years, a great deal of progress has been made
in developing quantitative models to do so (Boyce,
1992), and some of these have been applied to diadromous species (cf. Wainwright and Kope, 1999). This
general approach referred to as population viability and
analysis (PVA), can be quite powerful, but uncertainties
407
associated with parameter estimation and model choice
have limited their usefulness to date. Practitioners must
be cautious of model predictions having such low precision to render them useless. Furthermore, most PVA
models are based on demographic and population
dynamic processes of individual populations. Although
some PVA models have made an attempt to incorporate
genetic and/or metapopulation effects, a comprehensive,
fully-integrated PVA model that incorporates all significant risk factors remains an illusive goal. Therefore,
qualitative approaches, together with professional
judgement, are likely to remain important for the
foreseeable future.
Evaluating extinction risk for anadromous Pacific
salmonids poses some complex challenges. A practical
list would include: (1) How can extinction risk for
conservation units that are composed of many local
populations best be evaluated?; (2) On what temporal
and spatial scales are populations connected by migration and gene flow?; (3) How does metapopulation
structure affect small-population demographic and genetic risks?; (4) How best can the genetic and ecological
risks from hatchery production be factored into an
overall risk analysis?; (5) When rivers are stocked with
hatchery fish, how can sustainability of the natural
population be evaluated?; and (6) What is the best way
to evaluate the contribution of large-scale climate
changes (e.g. decadal-scale cycles in ocean productivity)
to extinction risk for salmon populations, which
typically exhibit large fluctuations in abundance?
Wainwright and Kope (1999) describe an approach that
combines quantitative and qualitative elements to arrive
at an overall assessment of extinction risk for complex
conservation units of Pacific salmon.
Restoration and recovery
The challenge of avoiding extinction is a difficult one
paralleled by the challenges of restoring extirpated or
endangered populations. Foremost in any recovery
strategy should be understanding the genetic population
structure for the species of concern. Nielsen (1999)
describes the historical processes that has led to the
decline of Pacific salmon (Oncorhynchus spp.) at the
southern end of their range in North America and
commented on recovery strategies for these populations.
Artificial propagation of salmon has been used for
over 100 years as an alternative to conservation of
natural populations; however, more recently there has
been increased interest in its use in stock restoration.
Artificial propagation can be used for reintroductions
into inaccessible habitat, and it also has the potential to
reduce transient extinction risk by rapidly increasing
population size. A novel approach toward this latter end
is described by Dempson et al. (1999), who captured
408
B. Jonsson et al.
out-migrating juveniles from anadromous populations
of Atlantic salmon (Salmo salar) in Newfoundland,
transported the fish to a salt-water rearing facility,
reared them to maturity, and subsequently returned
them to the native stream to spawn as adults. The
overall result was positive, indicating that captive rearing may have some use as tool to assist stock restoration.
In the experiments, however, only 80% of the surviving
adults released into a fjord returned to their native river
for spawning, whereas 20% strayed to other nearby
rivers. To home successfully, salmon is believed to pick
up sequential cues during the outward migration for
navigational help during the return (Hansen et al., 1993;
Hansen and Jonsson, 1994). In the experiment of
Dempson et al. (1999) the smolts were captured 0.75 km
from the river outlet and the fish were trucked to the
rearing facility in the estuary. This migratory disruption
may be the cause of the high straying rate (Fleming
et al., 1997). Smolt transfers of a few hundred metres
have been found to influence the precision and timing of
the return migration of Atlantic salmon (Jonsson et al.,
1991, 1994), and smolt releases in rivers appear to give
the lowest rates of straying to other rivers. Thus, there is
also potential for improvements.
Artificial propagation will not by itself lead to recovery unless the fundamental problems that caused the
declines in the first place (or which are limiting recovery
now) are addressed. Even the best-run hatchery programme entails risks for natural populations, and these
risks must be balanced against potential benefits to
determine whether supplementation can be effective in
restoration schemes (Waples, 1999). There is still a great
deal we need to learn about this issue. However, as
discussed by Reisenbichler and Rubin (1999), the
empirical data are sobering: each of the controlled
studies that has examined this issue found that progeny
of hatchery fish were characterized by substantial reductions in fitness in the wild compared to progeny of wild
fish. This raises the possibility that at least some wellintentioned supplementation programmes may do more
harm than good, and that healthy populations could be
transformed into a state in which they must depend on
continued hatchery supplementation for their persistence. Improved techniques of fish culture, release strategies, etc., can help to reduce deleterious effects of fish
culture, but they cannot be avoided altogether (Waples,
1999).
Finally, Lichatowich et al. (1999) point out that the
basic causes of the decline of Pacific salmon (habitat
degradation, overfishing, blockage of migratory routes
by dams) have been understood for over a century.
However, this knowledge has not prevented depletion of
the resource, which suggests that institutional processes
associated with fishery management have prevented
effective conservation measures from being enacted.
This simple realization indicates that, if meaningful
recovery of diadromous fishery resources is to occur,
biologists, managers, and society as a whole must fundamentally change the way species are perceived in the
ecosystem and in social contexts.
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