Individual, Population, Community, and
Ecosystem Consequences of a Fish Invader in
New Zealand Streams
COLIN R. TOWNSEND
Department of Zoology, University of Otago, 340 Great King Street, Dunedin, New Zealand,
email colin.townsend@stonebow.otago.ac.nz
Abstract: Knowledge of the population biology of invading species will often be necessary to develop effective
management procedures and policies. But because invaders can have unexpected indirect effects in food
webs, invasion ecologists need to integrate processes at the population level and other ecological levels. I describe a series of coordinated studies in New Zealand streams that address the effect of an exotic fish on individual behavior, population, community, and ecosystem patterns. Such case studies are important as an aid
to the formulation of policy about invasions that are especially likely to become problematic. At the individual level, grazing invertebrates showed changes in behavior as a result of the introduction of brown trout
(Salmo trutta), a predator that exerts a very different selection pressure than do native fish. At the population
level, trout have replaced nonmigratory galaxiid fish in some streams but not others, and have affected the
distributions of crayfish and other large invertebrates. At the community level, trout have suppressed grazing
pressure from invertebrates and are thus responsible for enhancing algal biomass and changing algal species
composition. Finally, at the ecosystem level, essentially all annual production of invertebrates is consumed by
trout (but not by galaxiids), and algal primary productivity is six times higher in a trout stream. This leads,
in turn, to an increased flux of nutrients from the water to the benthic community. The trout invasion has led
to strong top-down control of community structure and ecosystem functioning via its effects on individual behavior and population distribution and abundance. Particular physiological, behavioral, and demographic
traits of invaders can lead to profound ecosystem consequences that managers need to take into account.
Consecuencias de un Pez Invasor sobre Individuos, Poblaciones, Comunidades y Ecosistema en Arroyos de Nueva
Zelanda
Resumen: Para desarrollar procedimientos y políticas de manejo efectivos a menudo será necesario conocer
la biología de la población de especies invasoras. Sin embargo, debido a que los invasores pueden tener efectos indirectos inesperados en las redes alimenticias, ecólogos de invasión necesitan integrar procesos en la población y otros niveles ecológicos. Describo una serie de estudios coordinados en arroyos de Nueva Zelanda
que enfocan el impacto de un pez exótico sobre los patrones de comportamiento individual, de la población,
la comunidad y el ecosistema. Tales estudios de caso son importantes como un auxiliar para la formulación
de políticas sobre invasiones que pueden ser especialmente problemáticas. Al nivel individual, los invertebrados que pastorean mostraron cambios de conducta como resultado de la introducción de la trucha café
(Salmo trutta), un depredador que ejerce una presión de selección muy diferente a la de los peces nativos. En
el nivel de población, las truchas han reemplazado a peces galaxídos no migratorios en algunos arroyos pero
no en otros y han afectado las distribuciones de cangrejos de río y otros invertebrados mayores. Al nivel de
comunidad, las truchas han suprimido la presión de pastoreo por invertebrados y por lo tanto son responsables del incremento de la biomasa de algas y del cambio en la composición de especies de algas. Finalmente,
a nivel de ecosistema, la producción anual de invertebrados esencialmente es consumida por las truchas
(pero no por galaxídos), y la productividad primaria de algas es seis veces mayor en arroyos con truchas. A
su vez, esto conduce a incrementos en el flujo de nutrientes del agua hacia la comunidad béntica. La inPaper submitted January 16, 2002; revised manuscript accepted September 13, 2002.
38
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Volume 17, No. 1, February 2003
Townsend
Multilevel Effects of a Fish Invader
39
vasión de truchas ha conducido a un fuerte control de arriba hacia abajo de la estructura de la comunidad
y del funcionamiento del ecosistema por medio de sus efectos sobre la conducta individual y la distribución y
abundancia de la población. Las características fisiológicas, de conducta y demográficas particulares de los
invasores pueden llevar a consecuencias profundas en los ecosistemas que los administradores necesitan
tomar en consideración.
Introduction
A robust theory of invasion biology should provide a basis for rational decisions about which species are safe to
import and which accidental species introductions
should take priority in eradication efforts ( Townsend
1991). Understanding the population biology of invaders will often, but not always, be a prerequisite for devising appropriate management actions (Simberloff 2003
[this issue]). However, our understanding of the effects
of exotic species is still rudimentary. Not surprisingly,
we know most about the direct and dramatic consequences of invaders, although indirect consequences at
the community level have been the subject of recent
work (Culver & Kuris 2000; Louda 2003 [this issue]).
Studies of the ecosystem consequences of invaders have
been especially rare (but see, for example, Vitousek et al.
1987; Heath et al. 1995).
Ecology deals with individual organisms, populations
of organisms of a single species, communities of cooccurring species populations, and ecosystems, where
the focus is on the flux of matter and energy. It is unusual for ecological studies to encompass more than one
or two of these four levels. For most of this century,
physiological and behavioral ecologists, population dynamicists, and community and ecosystem ecologists have
tended to follow separate paths and ask different kinds of
questions. Individuals, populations, and communities all
exist in ecosystems, however, and our understanding can
be expected to be enhanced considerably when the links
between the levels are made clear ( Jones & Lawton 1994).
This is especially important in the case of invasions
because the population biology of the exotic species represents only a small part of the story. Population consequences might, in some cases, provide little cause for concern, whereas a more detailed knowledge would point to
far-reaching changes to ecosystem functioning.
I reviewed a decade-long series of studies on the effects
of brown trout (Salmo trutta) in New Zealand streams to
throw light on the way an exotic fish can influence every
aspect of the ecology of the ecosystem it invades. A sustained effort was made by acclimatization societies to introduce brown trout for angling into almost every accessible
water body. The species was introduced to the South Island of New Zealand beginning in 1867, and self-sustaining
populations are now found in many streams, rivers, and
lakes in the region (McDowall 1990; Townsend 1996).
Compared with many other invaders, few would make
the case that the brown trout has negative economic effects. On the contrary, the recreational salmonid fishery
in New Zealand, of which the brown trout is the prime
component, is conservatively valued at more than U.S.$300
million per year (N. Watson, personal communication).
We do not know whether trout have had a significant impact on New Zealand’s economically important native
freshwater fisheries (principally eels and whitebait, the
latter consisting of juveniles of various diadromous species of Galaxias). From the point of view of biodiversity, there is no evidence of a global extinction resulting
from the introduction of the trout to New Zealand, but it
has been responsible for local extinctions of native fishes
(Minns 1990; Crowl et al. 1992) and invertebrates (Whitmore et al. 2000).
No systematic records exist of a brown trout invasion
in action. Our approach takes advantage of the fact that
trout have colonized some streams but not others. Thus,
the current ecology of streams containing trout, as opposed to the previous occupants—nonmigratory (nonwhitebait), native fish in the genus Galaxias—allows us
to infer much about the impact of the trout invasion. Our
studies have been carried out in tributaries of the Taieri
River and the nearby Shag River in the south of New
Zealand’s South Island. When work began in 1989, only
one species of nonmigratory galaxiid, Galaxias vulgaris,
was considered to occur in these rivers. Recent studies
in the Taieri River, using isozyme electrophoretic and
mtDNA analyses, have led to the reinstatement of G.
anomalus (Allibone et al. 1996), previously synonomized
with G. vulgaris (McDowall 1970), and the establishment
of the new species G. depressiceps and G. eldoni ( McDowall & Wallis 1996; McDowall 1997 ). G. vulgaris is
present in the Shag River but not in the Taieri River. Almost invariably, only a single species of Galaxias occurs
at a site (only a single tributary is occupied by two species, G. depressiceps and G. anomalus ; Allibone &
Townsend 1997a). All the nonmigratory species are closely
related and have similar morphologies, behaviors, and
habitat requirements (Allibone & Townsend 1997b, 1998;
Moore et al. 1999), and their relationships with brown
trout are usually indistinguishable. In this review, I identify the actual species now known to have been present
in the earlier studies.
My aim is to highlight the way that details of the physiology, behavior, and life history of an invader may ac-
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Multilevel Effects of a Fish Invader
Townsend
count for effects at the individual, population, community, and ecosystem levels of the habitats they invade. I
also present evidence consistent with evolved responses
of native species that may be partly responsible for an
ecosystem-level impact of brown trout.
Impacts at the Individual Level
The arrival of trout has affected invertebrate feeding behavior. Nymphs of mayflies in the genera Nesameletus
and Deleatidium commonly graze on microscopic algae
growing on the beds of New Zealand streams. Observations of the diurnal activity of nymphs from galaxiid and
trout streams have revealed some striking differences.
Nesameletus ornatus collected from a trout stream and
placed, without fish, in small, artificial laboratory stream
channels were less active during the day than at night, in
contrast to those collected from a G. eldoni stream (McIntosh & Townsend 1994; Fig. 1a). Deleatidium from the
Shag River (where both trout and G. vulgaris occur)
were also more nocturnal when trout, rather than G.
vulgaris, were present (Fig. 1b).
A field-based study of Deleatidium provided further evidence of a profound behavioral difference in five matched
pairs of streams containing trout or galaxiids (G. eldoni or
G. depressiceps) (McIntosh & Townsend 1995a). A gutfluorescence technique revealed that the mean ratio of
algal pigments in night and day mayfly gut samples from
galaxiid streams was not different from unity (0.968 0.085), expected if the mayflies forage equally during day
and night. In contrast, the ratio in trout streams was significantly greater than unity (1.483 0.21).
In a further experiment, records were made of Deleatidium visible during late afternoon on the surface of
cobbles in artificial channels placed in a tributary of the
Shag River (McIntosh & Townsend 1996). The daytime
activity of Deleatidium, which occurred at similar densities in all channels, was significantly reduced in the presence of either fish species, but to a greater extent when
trout were present (Fig. 1c). In this experiment, six algacovered cobbles were introduced into each channel to
provide patches rich in food, and other cobbles were
scrubbed to create patches poor in food. Two days later
in the G. vulgaris channels, Deleatidium were 2.5 times
more abundant on rich than poor patches, whereas in
the trout channels abundance was the same on rich and
poor patches. The reluctance of mayflies to move when
trout are present prevents expression of an aggregative
response and further restricts foraging by Deleatidium.
Other researchers have shown that Deleatidium, as well
as snails and certain caddisfly larvae, have a lower propensity to enter the drift in a trout stream than a G. eldoni stream ( Williams 2000), and Drinnan (2000) has
reported reduced nocturnal drift by Deleatidium in
response to trout chemical cues.
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Volume 17, No. 1, February 2003
Figure 1. Mean number (SE) of (a) Nesameletus ornatus mayfly nymphs collected either from a trout
stream or a galaxiid stream that were recorded by
means of video as visible on the substrate surface in
laboratory stream channels during the day and night
(in the absence of fish) (after McIntosh & Townsend
1994); (b) Deleatidium mayfly nymphs in the camera’s field of view during laboratory trials with different fish predators during day and night (after McIntosh & Townsend 1996); and (c) Deleatidium nymphs
observed on the upper surfaces of cobbles during late
afternoon in channels (placed in a real stream) containing no fish, G. vulgaris, or trout (after McIntosh &
Townsend 1996).
Townsend
Multilevel Effects of a Fish Invader
41
Impacts of Brown Trout at the Population Level
Trout have affected the distributions of native fishes, crayfishes, and macroinvertebrates. For example, in a multitributary study (December 1989 to March 1990), Taieri
sites were classified as containing (1) no fish, (2) Galaxias only, ( 3 ) trout only, or (4) both Galaxias and trout
(Townsend & Crowl 1991). Multiple discriminant-functions analysis was used to determine which of several
physical variables could reliably discriminate between the
four fish classes. Trout occurred almost invariably below
waterfalls that were large enough to prevent their upstream migration (at least 3 m high) and at low elevations,
because sites without waterfalls downstream tended to
be at lower elevation. Sites containing G. depressiceps,
G. eldoni, or G. anomalus (or with no fish) were always
upstream of one or several large waterfalls. Re-analysis
of this 1990 database showed that, in allopatry, trout
generally attained lower densities than galaxiids (Fig. 2).
Despite lower densities, trout often had higher biomasses
than the galaxiids they replaced ( Fig. 3). On average,
Figure 3. Biomass (SE), assessed by successive electrofishing until no more fish were taken, of brown
trout and Galaxias spp. in allopatry and in sympatry.
The histogram labeled galaxiids represents all Galaxias
streams and species combined.
Figure 2. Density (SE), assessed by successive electrofishing until no more fish were taken, of brown trout
and Galaxias spp. in allopatry and in sympatry. The
histogram labeled galaxiids represents all Galaxias
streams and species combined. Densities in all cases
(except G. eldoni) were significantly higher in allopatry than sympatry (t tests, p 0.05).
trout achieved a biomass of 0.70 g ash-free dry weight
(AFDW )/m 2 in allopatry, whereas galaxiids achieved
0.39 g AFDW/m2. There is much variation, and these
means (t test) are not significantly different, but trout
were almost twice as likely as galaxiids to achieve a biomass of 0.75 g AFDW/m2 (C. J. Arbuckle & C.R.T., unpublished data). In sympatry, both trout and galaxiid
biomasses were lower (significantly so in the case of
galaxiids). The mean biomass of trout in sympatric populations was significantly higher than that of galaxiids.
The few sites that contained both trout and galaxiids occurred below waterfalls and at intermediate elevations,
and they had cobble beds. The unstable nature of these
streambeds may have promoted coexistence, but at
much-reduced densities (Fig. 2).
Brown trout are aggressive competitors, and G. vulgaris are excluded from preferred microhabitats when
trout are present ( McIntosh et al. 1992). Galaxiids also
make fewer successful predation attempts when trout
are in the vicinity (Edge et al. 1993). Thus, competition
may be partly responsible for the negative relationship
in the distributions of trout and native fish. The most
probable reason for the restriction of galaxiid populations to sites upstream of waterfalls, however, is direct
predation by trout on the native fish below the waterfalls. One small trout in a laboratory aquarium consumed
135 Galaxias fry in a day (C.R.T., personal observation).
In a study further north in the South Island, in which
brown trout and rainbow trout (Onchorhynchus mykiss)
were grouped for analyses and their distributions compared with a different set of galaxiid species, McIntosh
(2000) reported that trout and galaxiids did not coexist
where trout were longer than 150 mm (length from nose
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Multilevel Effects of a Fish Invader
to tail fork). His results indicate that exclusion of these
galaxiids depended on trout size and reflected the particular dominance of large trout as predators and/or
competitors. Re-analysis of the 1990 Taieri River database, however, reveals that the few sites where brown
trout and galaxiids were found together contained brown
trout whose maximum size was not significantly smaller
than that found at sites where trout occurred alone
(mean of maximum lengths [SE ]: 110.5 16.4 mm
and 127.2 7.2 mm fork length for trout in sites with
and without galaxiids, respectively; C. J. Arbuckle & C.R.T.,
unpublished data). Moreover, in two streams galaxiids
co-occurred with trout larger than150 mm, something
that was never recorded by McIntosh (2000). The different patterns may reflect the different ecologies of the
species involved or the details of the frequency of waterfalls or the nature of the bed-disturbance regime in the
Taieri and rivers farther north.
An apparent negative relationship between trout and
native freshwater crayfish was first suggested years ago
( Thompson 1922). In the Taieri River, the presence of
trout is negatively correlated with distribution of the crayfish Paranephrops zealandicus, both on a catchmentwide basis ( Whitmore et al. 2000) and at a local scale
within a single tributary ( Usio & Townsend 2000).
Shave et al. (1994) showed that these crayfish were unable to detect trout but used chemical cues to detect native eels.
Among the macroinvertebrates eaten by brown trout,
large, slow swimmers, including the mayflies Ameletopsis,
Oniscigaster ( Hudson 1904), and Nesameletus ( McIntosh & Townsend 1994), and large carnivorous invertebrates may be particularly vulnerable to trout predation.
In a channel experiment in the Shag River, Flecker and
Townsend (1994) found that large carnivorous invertebrates, including Archechauliodes diversus, are rarer
when trout rather than G. vulgaris are present. Similarly, in a survey of two Taieri tributaries, Huryn (1998)
reported that 9 of the 10 largest invertebrate species, including N. ornatus and A. diversus, are represented by
smaller individuals in the trout stream than in the G. eldoni stream, presumably a result of strong size-selective
predation.
Townsend
[McIntosh & Townsend 1996]), three treatments (no fish,
G. vulgaris present, or trout present) were established
in each of several randomized blocks separated by 50–
100 m in a 500- to 800-m stretch of the stream. Fish sizes
( 75–120 mm), densities, and biomasses fell toward the
high end of the natural range recorded in streams in the
region and were selected to provide identical densities and
similar biomasses of the two species in the channels. Algae and invertebrates were allowed to colonize the natural substrate within the channels for about 12 days before the fish were introduced. After another 12 days or
more, invertebrates and algae were sampled (Fig. 4).
The general patterns were similar in all three experiments, but there were some subtle differences. In the
first two experiments, a significant trout effect on invertebrate biomass was evident (analysis of variance; p 0.007 and 0.026, respectively), but the presence of
Galaxias did not depress invertebrate biomass in comparison with the no-fish control. In the third experiment
there were no significant differences in invertebrate biomass in any of the treatments. Algal biomass achieved its
highest values in the trout treatments of all the experiments, but this was statistically significant only in the
second ( p 0.02) and third ( p 0.008) experiments.
Why should essentially the same experiment produce
variable results? The most probable answer is that both
Impacts of Trout at the Community Level
The basal trophic level in these streams consists mainly
of periphyton that is grazed by various insect larvae,
which in turn are prey to carnivorous invertebrates; fish
are top predators. Experiments involving artificial, flowthrough channels placed into the Shag River have been
used to determine whether trout affect the stream food
web differently from G. vulgaris. In experiments performed on three occasions ( January 1992 and March
1992 [Flecker & Townsend 1994 ]; and February 1993
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Volume 17, No. 1, February 2003
Figure 4. Total invertebrate biomass and algal biomass (chlorophyll a) (SE) for experiments performed
on three dates in a small New Zealand stream. In the
first two experiments, algal biomass was estimated
from scrapings from the complete surface of cobbles,
whereas in the third experiment it was estimated by
scraping algae from the sides of cobbles (not bottoms
or tops)( after Flecker & Townsend 1994; McIntosh &
Townsend 1996.) Abbreviations: N, no fish; G, Galaxias
present; T, trout present.
Townsend
abiotic conditions (e.g., temperature, nitrate concentration in the water) and biotic conditions (algal and invertebrate species available to colonize the channels) differed between experimental periods. When the findings
are taken together, however, it is clear that trout do
have a more pronounced effect than G. vulgaris on invertebrate grazers and, consequently, on algal biomass.
The indirect effect of trout on algae occurred partly
through a reduction in invertebrate density (Fig. 4) but
also because trout restricted the grazing behavior of the
invertebrates that were present (Fig. 1c; results gained as
part of the experiment in February 1993). Evidence from
film records of grazing behavior (McIntosh & Townsend
1994), the width of grazing scars (Flecker & Townsend
1994 ), and the distribution of algae on the sides and
tops of stones in experimental channels (McIntosh &
Townsend 1996 ) all confirm that grazing invertebrates
spend less time out in the open and feed closer to refuges when trout are present. The reduced invertebrate
densities in two of the experiments may be a result of
higher predation rates by trout than galaxiids and/or a
greater tendency of invertebrates to leave (or not settle
in) channels containing trout (cf. Diehl et al. 2000).
These results constitute strong evidence of a trophic
cascade, with biomass of the plant trophic level increasing significantly when a key top predator (trout) is present.
In theory, this result is what is expected where there are
three (or some other odd number) trophic levels (Oksanen et al. 1981; Biggs et al. 2000). In fact, our stream
community has four trophic levels—fish, carnivorous invertebrates, grazing invertebrates, and algae—but it functions as a three-trophic-level system because trout are
direct exploiters of the grazing invertebrates (and carnivorous invertebrates, which are also their prey, have little
quantitative effect on grazing invertebrates).
In an attempt to confirm these patterns in natural situations, we assessed three pairs of streams, one containing trout and the other a galaxiid, for algal standing crops
and algal species composition (Biggs et al. 2000). In two
of the pairs of streams, the general rule applied, with the
biomass of trout being much higher than that of galaxiids (G. eldoni in one case and G. depressiceps in the
other). In the third pair of streams the biomass of the
two species was similar (uncharacteristically high for G.
depressiceps and somewhat low for trout). In all three
pairs of streams, the ash-free dry mass of the biofilm
of periphyton was, as predicted, greater in the trout stream
than the galaxiid stream. Moreover, the relative abundance
of prostrate algae was highest in the galaxiid streams.
These algal species, including Cocconeis sp. Cymbella
aspera, and Epithemia spp. are considered less vulnerable to grazing invertebrates (Steinman 1996) and can be
expected to be more prominent in streams where grazing is intense (i.e., as predicted for the galaxiid streams).
The relative abundance of erect algal species (including
Audouinella hermanii, Gomphoneis herculeana, and
Multilevel Effects of a Fish Invader
43
Synedra ulna), considered more vulnerable to grazing,
was higher in the trout case in two pairs of streams but
was similar in the third pair, where trout and galaxiid
biomasses were similar. These results provide further
support for the cascading influence of invading trout,
but they also indicate that the consequences of the invasion may depend, at least in part, on the tendency for
trout to establish a higher biomass in the streams than
the galaxiids they replace.
The negative effects of trout on crayfish deserve some
comment. This is because the crayfish Paranephrops
zealandicus can be considered a keystone species, influencing physical processes, such as sedimentation, and
biotic processes through consumption and bioturbation
(Usio & Townsend 2000; Whitmore et al. 2000; Hollows
et al. 2002). Both descriptive and experimental studies
in the Taieri River have shown that crayfish are responsible for a trophic cascade involving negative effects on
carnivorous invertebrates ( Tanypodinae midge larvae)
and consequent positive effects on their prey (Chironominae) (Usio 2000; Usio & Townsend 2000). In addition, the omnivorous crayfish have strong direct effects
on the abundance of algae and particulate organic matter through direct consumption and bioturbation (Usio &
Townsend 2000, 2001). Crayfish can be considered ecosystem engineers ( Jones et al. 1994), and any impacts of
trout on crayfish are likely to have profound knock-on
effects in the community.
Impacts of Trout at the Ecosystem Level
A strong trophic cascade, such as that produced by the
introduced brown trout, may be expected to have consequences at the ecosystem level, but this has not been
documented before, for two likely reasons. First, it is difficult to find two communities with contrasting predation regimes but the same physical settings. Second, a
particularly large effort and expense is required for such
studies (with the added problem that replication of
treatments is usually not feasible).
The sequence of studies described above provided the
impetus for a detailed energetics investigation of two
neighboring tributaries of the Taieri River with very similar physicochemical conditions, one occupied only by
trout and the other (because of a waterfall downstream)
only by G. eldoni ( Huryn 1998). No other fish were
present in either stream. As predicted, net primary production in the trout stream was consistently higher
throughout the year than in the G. eldoni stream (Huryn
1998), and annual net primary production was six times
greater in the trout stream ( Fig. 5). Secondary production—the rate at which consumers produce new biomass per unit area per unit time—by grazing invertebrates in the trout stream was about 1.5 times the rate in
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Multilevel Effects of a Fish Invader
the galaxiid stream, whereas trout themselves produced
new biomass at roughly nine times the rate of G. eldoni
(Fig. 5).
The results suggest that G. eldoni consumed only about
18% of available prey production each year, whereas the
grazing invertebrates consumed about 75% of primary
production in the galaxiid stream. In stark contrast, trout
consumed virtually 100% of annual invertebrate production in their stream, whereas the grazing invertebrates
consumed only about 21% of primary production ( Fig.
5). This is precisely what was predicted: strong topdown control of invertebrates by trout and release of the
algae to produce and accumulate biomass at a fast rate
(presumably limited only by available nutrients and the
rate at which algal cells are sloughed off during flow disturbances). In other words, there was an annual surplus
of algal production (in excess of demand of grazing invertebrates) in the trout stream which was almost 20
times as great as the estimated surplus in the galaxiid
stream. One can assume that the surplus dies and is
sloughed off from the surface of the streambed as fine
particulate organic matter to be consumed, at some distance downstream, by microorganisms and detritivorous
invertebrates. Thus, the ecosystem effect of the trophic
cascade may be felt at some distance from the location
of the trout.
The densities of trout and galaxiids in the two streams
were similar, but the biomass of brown trout was six
times as great as that of galaxiids. Regardless of the various underlying mechanisms leading to a trophic cascade, the difference in biomass will contribute further to
a large trout effect. In another pair of streams, one containing trout and the other ( because of a downstream
waterfall) containing G. depressiceps, a higher rate of uptake of ammonium, nitrate, and phosphate from stream
Figure 5. Annual production estimates for primary
producers (algae), invertebrates, and fish in a G. eldoni stream (G) and a neighboring trout stream (T)
(after Huryn 1998). The proportion of annual production needed to satisfy the demand of consumers at the
next level is shown by shaded histograms.
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Townsend
water was recorded in the trout stream, as is to be expected if algal production is enhanced in the presence
of trout (K. Simon and C.R.T., unpublished data).
Discussion
Community and Ecosystem Consequences that Depend on the
Novel Behavior of an Invader
The native nonmigratory galaxiid species in the Taieri
and Shag rivers can cause a weak trophic cascade (perhaps better termed a trophic trickle; Strong 1992). In our
experiments, there was sometimes an increase in algal
biomass in the presence of galaxiids compared with situations without fish, but brown trout had much more profound and predictable effects. Brown trout forage from
positions in the water column, rely principally on vision,
and are more likely to capture prey during the day. The
galaxiid species, on the other hand, forage at the streambed,
seem to use mechanical cues to detect prey, and consume
similar numbers of prey during day and night (McIntosh &
Townsend 1995b, 1998). It may be that visual predators
are generally more likely to cause a trophic cascade because they not only have the potential to reduce the
density of their prey but also to limit their activity. Such
an effect will be particularly marked if an invader that is
a visual predator is introduced to a native community
that has historically lacked such predators, such as in
New Zealand. The magnitude of the trophic cascade,
and its clear consequences for ecosystem productivity
and nutrient flux, also depend on the rapid response of
algal primary producers to variations in grazing pressure
caused by the invader.
Studies of salmonid invaders of previously fishless lakes
provide an intriguing contrast to brown trout in New
Zealand streams. Salmonid introductions may lead to declines in large-bodied zooplankton populations in
lakes (McNaught et al. 1999) and shifts in their distributions to less vulnerable locations in deeper water (Gliwicz & Rowan 1984), effects that parallel the individual
and population consequences of brown trout in streams.
The consequent reduction in grazing is also no doubt
partly responsible for increases to phytoplankton biomass and productivity in previously fishless North American lakes (Leavitt et al. 1994; Schindler et al. 2001). But
the tendency of invading salmonids such as rainbow
trout (Onchorhynchus mykiss) to feed on benthic and
littoral invertebrates and to excrete nutrients in the pelagic zone leads to the enhancement of phosphorus flux
to the latter. Schindler et al. (2001) argue that this is the
principal mechanism for increased phytoplankton productivity. Salmonid introductions to lakes provide a further example where understanding of the ecosystem consequences of an invader depends on knowledge of
individual behavior and population-distribution patterns.
Townsend
Evolutionary Consequences among Native Species Resulting
from an Invasion
The arrival of brown trout in some streams but not others
is associated with inflexible, presumably evolved, differences in the behavior of the mayfly (Nesameletus ornatus), believed to be particularly vulnerable to trout because of its large size and tendency to swim slowly in
the water column. The inflexible nature of this strategy,
even in the complete absence of all physical and chemical cues from the predator, indicates that it may have become fixed or canalized (Sih 1987; Stearns 1989). On
the other hand, there is no indication that the positioning response of Deleatidium to trout is fixed. In the
field experiments in the Shag River, for example, where
both trout and G. vulgaris occur, Deleatidium were more
likely to remain in their refuges during the day when
trout were in the vicinity. Such a flexible response is
characteristic of other parts of the world where native
salmonid fish occur (e.g., Cowan & Peckarsky 1993;
Douglas et al 1994; Tikkanen et al 1996; McIntosh et al.
1999 ). Whether fixed or flexible, the response of grazers contributes to the strength of the trophic cascade induced by the invader. In the case of the crayfish P.
zealandicus, a much larger native species with a longer
generation time, the animals are apparently unable to
detect trout chemically but can detect and respond to a
native predator, the eel Anguilla dieffenbachii (Shave
et al. 1994). The lack of an evolved ability to detect the
invading trout may be a contributory factor in the local
extinction of crayfish.
Community and Ecosystem Consequences of an Invader’s
Life-History Traits
Although trout characteristically achieve lower densities
than the galaxiids they have replaced, they often achieve
a higher biomass. This doubtless contributed to the size of
their impact in Huryn’s (1998) energetics study. Huryn’s
two streams were chosen for study because they both
held excellent populations of fish and were located in
adjacent and physically similar catchments. From experiments in which fish density and biomass were controlled,
we know that trout nevertheless cause a strong trophic
cascade, but the ability to achieve a higher biomass is a
further factor of importance.
A physiological contribution to achieving high biomass
would occur if trout were to have higher assimilation and/
or net growth efficiencies than galaxiids. Whether trout are
more efficient than galaxiids at assimilating food and converting assimilate into body tissue is worthy of investigation. At the level of the individual organism, both physiological and behavioral characteristics have the capacity to
strengthen the impact of an invader.
Other life-history features may also contribute to trout attaining a higher biomass. It may be that recruitment by
Multilevel Effects of a Fish Invader
45
trout is more regular than by galaxiids, or trout mortality
from one year-class to another is lower, or recolonization of
sites by trout after disturbance is faster. Huryn (1998) collected stream data for 5 years. During this period there was
a steady decline in G. eldoni population size associated
with high spring and summer discharge, which seemed to
remove many of the “pelagic” young of the year. This was
reversed only by 1 year of massive recruitment when flow
conditions were less extreme ( A.D. Huryn, personal
communication). The vulnerability of these nonmigratory
galaxiids to high discharge during the recruitment period
may be a ghost of diadromy past: their ancestors migrated
as pelagic larvae to estuaries and oceans ( Waters et al.
2000; Waters & Wallis 2001). Trout hatch later, are probably less vulnerable in their redds to high-flow events, and
generally show more consistent recruitment from year to
year (A.D. Huryn, personal communication).
An invasion by brown trout of galaxiid streams provides
a stark contrast to the invasion by mosquitofish (Gambusia affinis) of Arizona desert streams containing native topminnows (Poeciliopsis occidentalis) (Meffe 1984). Mosquitofish typically eliminate topminnows from native habitats
by predation within about 3 years. In streams subject to frequent floods, however, the topminnow persists because it
is better fitted to survive the floods than the mosquitofish,
which evolved in lowland drainages with very different hydrological regimes. In the Arizona streams, the invader
fares less well than the native fish in the typical disturbance
regime. Ironically, brown trout seem better fitted to withstand high-discharge events in the New Zealand streams
than the native galaxiids. The prediction of invader effects
requires understanding of the species’ response to both
“normal” environmental conditions and to prevailing disturbance regimes.
Mortality data for brown trout in our streams is lacking, but it is of interest that the practice of importing
trout as ova is apparently responsible for the fact that
only 17 parasites are associated with trout in New
Zealand as opposed to 63 in the United Kingdom (Boustead
1982 ). Perhaps trout mortality is lower as a result of
lower parasite burdens. However, levels of productivity
achieved by trout in New Zealand appear to be only as
high as those recorded in productive situations elsewhere in the world (Huryn 1998). We lack comparative
data on recolonization potential, but in their headwater
fastnesses above waterfalls galaxiids are likely to be
slower than trout to recolonize after a population decline. Trout also may be able to achieve a higher biomass because they are longer lived and grow to a larger
size. Whatever the precise mechanism, trout seem consistently able to build populations to the point where
food limitation occurs, whereas galaxiids do not (Huryn
1998). A thorough knowledge of the life histories and
population dynamics of invaders and native species
seems to be a prerequisite for appropriate conservation
decisions.
Conservation Biology
Volume 17, No. 1, February 2003
46
Multilevel Effects of a Fish Invader
Conclusions
These unusually comprehensive studies of brown trout
provide an example of how the “natural experiments”
provided by invaders can be used to elucidate fundamental ecological questions (Simberloff 2003 [this issue]).
The applied significance of our results is limited, partly
because brown trout are so highly valued but also because of the intractable problem of removing them from
most locations. Nevertheless, managers need to identify
and protect native fish refuges above migration barriers.
This requires that landowners and anglers be made fully
aware of the impact of trout on vulnerable native species and of the need to prevent their further spread.
Some migration barriers have been breached in the past
when trout were deliberately introduced to upstream locations. Such situations provide opportunities for the local removal of brown trout and the reintroduction of
nonmigratory galaxiids. From another point of view, my
synthesis provides the necessary underpinning for importation decisions: the New Zealand government decided
not to import channel catfish (Ictalurus punctatus) for
aquaculture partly because of our knowledge of brown trout
and of the similar risks posed by the catfish (Townsend &
Winterbourn 1992). When deciding whether to introduce
a potentially beneficial invader or to eradicate or contain
an unwanted invader, managers need to beware of invaders whose ecological role is novel, those that are
likely to interact with keystone native species or to influence key ecosystem processes, and those that are likely
to establish higher densities or biomasses than the native species they may replace. Progress in invasion ecology also requires that we pay attention not only to the current ecologies of invading species and native communities
(Lodge 1993) but also to the potential consequences of
natural selection acting on invaders and natives to reshape the outcome (Townsend 1996). In the final analysis, however, even profound ecological effects may
prove to be economically insignificant if the introduced
species is valued and the functioning of the native ecosystem is not.
Acknowledgments
The body of work I reviewed is the product of a series of
dedicated researchers with a single long-term objective.
Particular thanks goes to T. Crowl, A. Flecker, A. McIntosh, A. Huryn, B. Biggs, K. Simon, and C. Arbuckle.
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