J. Appl. Ichthyol. 21 (2005), 263–274
2005 Blackwell Verlag, Berlin
ISSN 0175–8659
Received: April 16, 2005
Accepted: June 24, 2005
Pathways of ornamental and aquarium fish introductions into urban ponds of Epping
Forest (London, England): the human vector*
By G. H. Copp1, K. J. Wesley2 and L. Vilizzi3
1
CEFAS, Salmon & Freshwater Team, Lowestoft, Suffolk, England; 2Bedwell Fisheries Services, Welham Green, Hertfordshire,
England, UK; 3Viale Italia, Sassari, Italy
Summary
To examine the role of humans in the non-native fish
introductions, we measured the frequency of occurrence and
density of non-native fishes in ponds (Epping Forest, Essex,
England) that had been restored (drained of water and voided
of fish or treated with rotenone) on a known date and into
which no piscivorous or non-native fishes had subsequently
been stocked intentionally. For each pond, the period of time
since pond restoration, pond area, distance to nearest residential housing, distance to nearest footpath, distance to nearest
water body or stream, and the proportion of pond vegetated
were measured. The occurrence of both non-native and
unexpected native fish species was non-random, and the
number of ornamental varieties was found to increase as pond
distance from the nearest road decreased. Variety richness of
each of three categories of fish (non-native, goldfish Carassius
auratus and native) was significantly correlated with at least
two of the following variables: distance from nearest road,
nearest footpath and nearest pond. The rate of non-native fish
introductions (adjusted variety richness per year) could also be
estimated from pond distance to the nearest road, being about
3.5 ornamental varieties introduced per year in ponds adjacent
to roads, but the rate appears to be much greater in ponds that
had recently (<1.5 years) undergone restoration. Implications
for conservation and management, as well as the potential role
of societal issues such as recreational activities, cultural and
religious practices, are discussed.
Introduction
The introduction of ornamental fish to Europe began in the
17th century (Lever, 1996), initially of goldfish Carassius
auratus and possibly its close congener, gibel carp C. gibelio
(see Copp et al., 2005). Similar to common carp Cyprinus
carpio, which had been introduced to the UK in the 15th
century, goldfish were introduced mainly into ponds and small
lakes, which are now known to be particularly important in
sustaining aquatic species diversity (Steiner, 1988; Oertli et al.,
2002; Williams et al., 2003). Natural ponds have become less
common in the UK over the last two centuries, but this was
matched by an increase in the number of artificial ponds for
ornamental and water supply purposes. The colonization of
Ônewly formedÕ water bodies has long attracted the interest of
scientists (e.g. Darwin, 1859) as a means of understanding
*This paper is dedicated to the memory of Mr. Alwyn Wheeler: friend,
colleague and champion of both our native crucian carp and the ponds
of Epping Frest.
U.S. Copyright Clearance Centre Code Statement:
species dispersal mechanisms, colonization rates (propagule
pressure) and establishment success (Kew, 1893; Talling,
1951). However, ponds are increasingly threatened by changes
in land use and by releases of non-native species (Semlitsch
and Bodie, 1998). Of particular concern are the potential
impacts of non-native species (Andrews, 1990; Wheeler, 1991;
North, 2000), and some studies suggest that impacts may be
enhanced in ecosystems subjected to human alteration (Fox
and Fox, 1986; Meffe, 1991).
Demonstrated effects of goldfish introductions involve the
native European crucian carp Carassius carassius (Wheeler,
2000; Navodaru et al., 2002). Previously believed to have been
introduced along with common carp (e.g. Maitland, 1972),
crucian carp was re-classified in the 1970s as native to southeastern England, based on archaeological evidence and the
similarity of the crucian carp’s pre-1960 distribution to that of
other native cyprinids (Wheeler, 2000; Wheeler et al., 2004).
As elsewhere in Europe (see Copp et al., 2005), crucian carp
populations in England are in decline because of habitat loss
(Copp, 1991; Everard et al., 1999) as well as reproductive
interference, i.e. hybridization, gynogenesis (Wheeler, 2000;
Vetemaa et al., 2005) and associated genetic variability (Tóth
et al., 2005). Threats to crucian carp have been exacerbated by
its physical similarity to the brown variety of goldfish, which
has been mistaken for crucian carp during fish transfers in the
UK (North, 2000; Wheeler, 2000) and fisheries catches
elsewhere (Vetemaa et al., 2005).
Despite the considerable trade in ornamental fishes
(Andrews, 1990; Crossman and Cudmore, 1999), which in
the UK averages out to about 22 fish per household (OATA,
2004), the release and dispersal of ornamental fishes have
received little attention worldwide (e.g. Kahn et al., 1999;
Duggan et al., 2005). Indeed, although pet fish releases to open
waters have been attributed to the general public (Wheeler,
2000), the pathways and mechanisms associated with these
introductions, and the rates at which they occur, remain
virtually unstudied. Managed, artificial ponds in urban areas
may be subject to rehabilitation management (draining,
desilting, refilling), which provide an opportunity to examine
the patterns of fish introductions and to estimate colonization
rates (Talling, 1951). The aim of the present study was thus to
examine the factors associated with pond colonization by nonnative fishes and the implications for the conservation of
native species, in particular crucian carp. Our specific objectives were to: (i) test whether the occurrence of non-native fish
varieties in restored ponds is random (i.e. Ôchance elementÕ,
Talling, 1951); (ii) test for relationships between geographical
features and ornamental fish occurrence (number and relative
0175–8659/2005/2104–0263$15.00/0
www.blackwell-synergy.com
264
density); (iii) estimate the rate at which non-native fishes are
introduced; and (iv) compare our data from Epping Forest
with published information (Wheeler, 1998) to identify trends
and clues as to the propensity for non-native fish introductions, including Wheeler’s observation that ponds adjacent to
fair grounds are likely introduction sites for goldfish given
away as fairground prizes.
Study area
Epping Forest, situated in the north-eastern part of Greater
London (Fig. 1), encompasses over 24 km2 and consists of
semi-natural woodland, grassland, scrub, heath, marsh and
water bodies (Conservators of Epping Forest, 2002). Most of
the Forest is registered as a Site of Special Scientific Interest,
the highest conservation status in England. Approximately 150
ponds have been recorded in Epping Forest. Besides crucian
carp, species of conservation interest associated with these
ponds include grey heron (Ardea cinerea), common (Triturus
G. H. Copp, K. J. Wesley and L. Vilizzi
vulgaris) and great crested (Triturus cristatus) newts. Within
the last 8 years, 18 of the ponds have undergone restoration,
which included the removal of the water, fish, rubbish,
ligneous debris and, if required, accumulated sediments to
abate eutrophication and terrestrialization processes (Conservators of Epping Forest, 2002). During pond restoration, the
removal of water was virtually complete, with only a single
small pool remaining where the sump pump was situated; this
pool was intensively fished with nets and electrofishing.
Although it is impossible to guarantee that all fish were
removed in fish eradications (e.g. Pot et al., 1984), the
probability of any fish surviving was extremely low. After
restoration, the ponds were usually left to refill naturally;
ponds were either not restocked with fish (to promote
amphibian populations) or restocking was restricted to one
or a few native species of conservation interest (i.e. crucian
carp, rudd Scardinius erythrophthalmus, tench Tinca tinca).
Ponds included in the present study were: (i) of full public
access; (ii) restored on a known date; (iii) voided of fish when
Fig. 1. Mapof Epping Forest (Essex,
England) with ponds included in the
study indicated by the number given in
Table 1
Introduction of ornamental fish into ponds
restored; and (iv) not restocked with fish or restocked with
known native, non-piscivorous species (Table 1). In one case
(Fairmead Pond), complete restoration was not deemed necessary and fish removal efforts (electrofishing and netting) were
followed by application of rotenone piscicide. In another case
(Bull’s Head Pond), approximately 30 goldfish were captured
within 2 months of pond restoration, with goldfish again
captured during two subsequent nettings (D. Huckfield, pers.
comm.). Following our visit, we learned that two large pike
(Esox lucius) had been introduced to eliminate the goldfish,
which were being introduced repeatedly by a nearby resident (D.
Huckfield, pers. comm.). We found only one small pike [18.4 cm
fork length (FL)], presumably a progeny of the introduced pike.
This site was therefore excluded from the analyses.
Materials and methods
For each pond, we recorded geographical features (distance in
m of the pond from the nearest road, footpath, residential
buildings, other water bodies/courses) as well as pond character [area in m2, age in years, connectivity with other waters,
mean depth in m, and the proportion (%) of the water body
occupied by aquatic vegetation]. All sites were sampled by
electrofishing using a generator-powered DC electrofishing
unit from a fibreglass boat powered by an electric motor.
Because of great variation in pond size, fish densities were
calculated on a catch per unit of effort (CPUE) basis (number
of fish per 10 min; see Murphy and Willis, 1996, p. 616) from
three ÔtimedÕ electrofishing passes undertaken from a fibreglass
boat or by wading at a similar speed of movement in all cases.
Exceptions were: (i) Oak Hill ÔwoodsÕ pond – only one pass by
wading was possible due to limited open water due to dense
aquatic vegetation over a thick layer of silty substratum, which
caused high turbidity once disturbed; and (ii) Jubilee Pond –
when routine sampling yielded no fish, a portable batterypowered backpack unit was used in the shallow margins to
confirm the complete absence of fish. Where possible, two
sweeps of a seine net (50 m length, 3 m depth, 0.9 mm mesh)
were undertaken in different parts of the pond to corroborate
the CPUE electrofishing results.
Immediately after capture, fish were identified to species and
ornamental variety, then measured for FL or total length
(threespine stickleback), with scale samples (from between the
lateral line and the dorsal fin) taken from a sub-sample of the
most common varieties for age determination. Because a
number of varieties of the same fish species, including native
species (e.g. golden rudd, golden tench), may be available in
the ornamental trade, we used the number of ornamental
varieties rather than the number of species as the measure of
richness (S). Both goldfish and common carp are biogeographically alien to the UK (see Copp et al., 2005) but have the
legal status of Ôordinarily residentÕ in England and Wales (i.e.
exemption from legislation pertaining to non-native freshwater
fish species); they are nonetheless categorized as non-native in
the present study. Fish density was estimated as catch per unit
of effort (CPUE: number of fish per 10 min of electrofishing).
We used length–frequency analysis (combined with scale
ageing of a sub-sample of specimens) to determine whether
population size and age structure were consistent with a
successfully reproducing population.
To test the randomness of fish occurrence, the observed
frequencies of non-native, goldfish and introduced native
varieties were subjected to the exact unconditional independence test (EUIT) for the multinomial model in 2 · 2
265
contingency tables (Berger, 1996). The EUIT is generally more
powerful than the Fisher exact test (Berger, 1996), which is
conditional and often fails to detect even moderately large
differences between two proportions when sample sizes are
small (Everitt, 1993). Furthermore, to increase the heuristic
value of the analyses, tests of significance were at a ¼ 0.10. As
six of the variables demonstrated binomial frequency distributions, deviations from expected occurrence were tested with
respect to pond area (pond area; small: <3000 m2, large:
‡3000 m2), percentage of the pond occupied by vegetation
(vegetation cover; sparse: <50%, dense: ‡50%), and distance
of the pond from the nearest water bodies (DPond; close:
<200 m, far: ‡200 m), from the nearest footpath (DPath;
close: <5 m, far: ‡5 m), from the nearest road (DRoad; close:
<25 m, far: ‡25 m), and from the nearest houses (DHouses;
close: <100 m, far: ‡100 m) (Table 1). The EUIT was
implemented through a Java applet at http://www.stat.ncsu.
edu/exact/tables.html (accessed 25 July 2005).
Measures of species richness (S) in wild fish populations are
known to be influenced by sampling effort and fish density,
therefore relationships between S and fish density and between
S and sampling effort were also determined by Poisson simple
regression models, and variety richness adjusted for fish
density (S¢). Relationships between geographical features
(Table 1) and S (or S¢) of non-native, goldfish and introduced
native varieties were subsequently assessed by Poisson multiple
regression (S-Plus, 2000). This is a special case of the
generalized linear model, and is useful for modelling counts
that typically follow a Poisson distribution (here evaluated by
the Kolmogorov–Smirnov test). The best combination of
independent variables was then determined by calculating the
change in deviance for the sequential addition of each variable,
using the chi-square test at a ¼ 0.10 for testing differences
between models. Relationships between geographical features
and S¢ as well as those with the density of non-native, goldfish
and introduced native varieties were assessed by robust
multiple regression (S-Plus, 2000). Robust regression models
are useful for fitting linear relationships when the random
variation in the data is not normal or when the data contain
significant outliers. In such situations, standard linear regression may return inaccurate estimates, whereas the robust MM
regression (Yohai, 1987) method returns a model that is almost
identical in structure to a standard linear regression model.
The significance (a ¼ 0.10) of the dependent variables was
then determined by the Wald test for sequential addition of the
terms. Of the geographical variables, pond area was of
particular interest for examining species–area relationships
(Connor and McCoy, 1979), of the form S ¼ cAz [S ¼ species (variety) richness; A ¼ pond area; c and z constants],
which were fitted to non-native, goldfish and introduced native
varieties by non-linear regression, and the validity of parameter estimates assessed by examination of Cook–Weisberg
confidence curves using SYSTAT v. 10.2. The resulting
individual fits were then compared by a modified analysis of
residual sum of squares (ARSS: Chen et al., 1992).
Multiple and simple linear regression were used to estimate
the rate at which non-native varieties were introduced (DSE).
Two of the geographical variables (i.e. DRoad, DHouses) have
changed little over the last 15 years and could be derived
cartographically with a high degree of confidence. Therefore,
data derived from Wheeler (1998) were subjected, where
possible, to the same tests of randomization and regression.
Although Wheeler’s data were collected using similar methods
to those we used, these were not applied in a CPUE manner.
Strawberry Hill
Johnson’s
St-John’s
Goldings Hill
Oak Hill ÔroadÕb
Oak Hill ÔwoodsÕ
Fairmead’sc
Bull’s Headd
Jubilee (Yacht’s)e
Bandstand
Carroll’s Farm
True Love’s
Alexandraf
Butler’s
Bomb crater 1g
Bomb crater 2h
Bomb crater 3h
Bomb crater 4i
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
TQ414965
TQ401920
TQ408941
TQ429981
TQ439992
TQ439993
TQ409966
TQ415955
TQ401862
TQ405859
TQ389967
TQ393975
TQ415863
TQ398948
TQ408964
TQ408964
TQ408963
TQ408963
NGR
21 March 2003
21 March 2003
25 March 2003
26 March 2003
26 March 2003
26 March 2003
31 March 2003
31 March 2003
21 May 2003
1 April 2003
8 April 2003
8 April 2003
28 July 2003
29 July 2003
29 July 2003
29 July 2003
29 July 2003
29 July 2003
Date sampled
March 2000
April 2002
April 2000
November 2001
September 1995
September 1995
October 1996
December 2000
August 2002
September 1995
September 1996
August 1998
March 1997
September 1996
September 1995
September 1995
September 1995
September 1995
Date restored
3.00
0.92
2.92
1.33
7.50
7.50
6.42
0.25
0.75
7.50
6.50
4.58
6.33
6.83
7.83
7.83
7.83
7.83
3000
800
12 498
4425
300
360
453
403
24 000
4200
706
196
80 000
731
11
12
14
9
Area (m2)
1.00
0.85
0.50
0.60
0.75
0.80
1.20
1.50
1.30
0.70
2.50
0.25
0.70
0.80
0.25
0.30
0.50
0.30
Mean depth
300
250
500
80
35
35
90
490
420
420
330
340
440
400
25
10
6
6
Pond
27.0
1.8
2.5
8.5
3.5
3.0
47.0
0.5
1.0
13.0
4.0
4.0
5.0
10.0
23.0
10.0
34.0
36.0
Path
Distance to nearest:
300.0
1.8
2.5
8.5
3.5
51.0
47.0
2.5
4.0
23.0
4.0
79.0
10.5
19.5
86.0
74.0
80.0
72.0
Road
450.0
12.0
25.0
30.0
11.8
62.0
760.0
9.5
60.0
40.0
3.0
220.0
21.0
660.0
640.0
640.0
640.0
640.0
Houses
2
24
1
22
76
77
90
3
1
61
95
36
1
58
70
95
95
90
Percentage
vegetation covera
a
Aquatic plants consisted of sedge Juncus spp., yellow flag iris (Iris pseudacorus), reed grasses (Glyceria spp.) + bullrushes (Typhus spp.), common reed (Phragmites australis), yellow lily (Nuphar lutea) and
ornamental varities such as white water lily (Nymphaea alba), aquatic mint (Menta aquatica), pondweeds (Potamogeton spp.).
b
Common newt present.
c
Rotenoned.
d
Goldfish sighted within months of cleaning, but two pike (about 1 kg) introduced in April 2002, hence excluded from analyses.
e
Data from second sampling visit used, many Canada geese on all occasions.
f
Signal crayfish (Pacifastacus leniusculus) captured by seine net.
g
Great crested newt present.
h
Cattle damage to banks.
i
Juvenile newts, cattle damage to banks.
Pond name
Site no.
Years
restored
Table 1
List of man-made ponds of Epping Forest (Essex, England) sampled during spring and summer of 2003, with their national grid reference (NGR), date sampled, date restored, years since restoration (restor.),
surface area, mean water depth (m), Distance (in m) to nearest water body (pond), footpath, road and residential area (houses), and the percentage of water surface occupied by aquatic vegetation
266
G. H. Copp, K. J. Wesley and L. Vilizzi
Introduction of ornamental fish into ponds
This restricted direct comparison with our CPUE data to
relative abundance (%) with respect to variety richness (S).
For comparisons with Wheeler’s (1998) non-CPUE data, S
could not be adjusted for fish density (S¢), but it could be
adjusted for sampling effort (S¢¢) by dividing the number of
varieties by the number of sites visited (used as a surrogate of
sampling effort) during three intervals of Wheeler’s (1998) data
(1992–1994, 1995–1996, 1997–1998) and for our data from
2003. To assess the progressive incidence of non-native
varieties during these intervals, an index of exoticness (IE)
00
was calculated as: IE ¼ SE00 =SN
, where SE00 is the adjusted non00
native variety richness and SN
is adjusted native variety
richness. We also used Jaccard’s coefficient of similarity,
JCS ¼ [a/(a + b + c)] · 100: where a is the number of
species present in both biotas, b the number of species present
only in the first biota, and c the number of species present only
in the second biota. JCS was calculated separately for nonnative and native species (varieties combined by species and
hybrids ignored) for each time interval described above (see
Rahel, 2002) to assess the temporal pattern of differentiation
vs homogenization using the ratio index: JCSE/JCSN, where
ratios <1 indicate differentiation and those >1 indicate
homogenization (McKinney, 2004).
Finally, we were able to assess Wheeler’s (1998) assumption that goldfish in ponds adjacent to fair grounds are likely
to receive goldfish as unwanted fairground prizes. Jubilee
Pond, created for the Queen’s Jubilee, was filled in August
2002 and purposely not stocked with fish. When no fish were
found during the initial sampling in early April 2003, the
pond was sampled about a month after the Spring Fair of
2003 (the first held next to the site since its creation), as well
as after two subsequent fairs held in early and late summer of
2003.
Table 2
List of species and varieties of native
and non-native fishes, the number of
specimens (n) captured in 18 ponds of
Epping Forest during March–August
2003 (Table 1), the frequency of
occurrence (f) in all ponds and the
numbers of fish (ornamental or fairground prize goldfish) abandoned/
introduced into Jubilee Pond sampled
initially (1 April) and as soon as
logistically possible after Bank Holiday weekend fairs (5 May, 26 May,
25 August). Fork length in cm given in
parenthesis for specimens not included
in Fig. 5
267
Results
Apart from the native threespine stickleback, the most
commonly encountered and most abundant fishes captured
in the ponds were varieties of fish not native to the British Isles,
in particular the brown and ÔredÕ varieties of goldfish and
varieties of common carp (Table 2). Approximately 50% of
both golden and brown goldfish were of the Ôfan-tailedÕ morph.
Successful establishment (reproduction) of goldfish varieties
following un-authorized introduction is evident in the length–
frequency distributions (Fig. 2). In Fairmeads Pond, one of
two ponds in which crucian carp were known to exist
(Wheeler, 1998), hybrids of goldfish with crucian carp occurred
in relatively high numbers (Table 2). A goldfish · ghost
(common) carp hybrid was also found (Jubilee Pond), having
been introduced into Jubilee sometime between 1 April and 21
May 2003 (see below).
The occurrences of both non-native and unexpected native
fishes in Epping Forest ponds were not random (EUIT), with
significant deviations from expected (Table 3) observed with
respect to DRoad and DHouses for non-native, goldfish and
unexpected native species/varieties, which were more abundant
in ponds close to roads and houses respectively. Further, there
were fewer unexpected native species/varieties in ponds close
to other water bodies.
Quantitatively, variety richness increased with sampling
effort (P < 0.001, 0.01, 0.05 in non-native, goldfish and
introduced native varieties respectively) and the rate of
increase was higher for non-native than for goldfish varieties
and introduced native species/varieties, in this order (see
Appendix 1 for details). A similar pattern was observed
between richness and fish density. With regard to S, reliable
estimators for non-native varieties are DRoad and DPath, for
goldfish varieties DRoad, DPath and to a lesser extent DPond,
Species/variety
Native
Threespine stickleback
Tench
Crucian carp
Rudd
Golden rudd
Roach
Non–native
Goldfish (golden)b
Goldfish (fairground size)
Goldfish (brown)b
Goldfish (shubunkin)b
Lion’s head goldfishb
Common carpb
Common carp (ghost)b
Common carp (koi)b
Common carp (ogen koi)b
Goldfish · ghost carp
Brown goldfish · common carp
Brown goldfish · crucian carp
Golden orfe (golden ide)
Topmouth gudgeon (clicker barb)
a
All sites
Jubilee Pond
n
f
1 April
21 May
24 Julya
28 August
229
113
17
46
1
1
22.2
5.6
5.6
11.2
5.6
5.6
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
286c
–
307
5
1
9
2
6
1
1
1
9
1
5
38.9c
–
27.8
11.1
5.6
22.2
11.1
11.1
5.6
5.6
5.6
5.6
5.6
5.6
–
–
–
–
–
–
–
–
–
–
–
–
–
–
1
2
–
–
–
–
1 (16.4)
–
–
1 (15.1)e
–
–
1 (14.5)
–
–
)a
186d
–
1
–
–
–
–
–
1 (19.0)
–
–
–
2
13
218d
–
–
–
–
–
–
–
–
–
–
–
Long delay in sampling after fair because of illness.
Biogeographically non-native and thus categorized as such despite their legal status in England and
Wales as Ôordinarily residentÕ.
c
Includes 30 goldfish captured in Bull’s Head Pond 2 months after restoration – this site excluded from
analysis due to subsequent introduction of a pike).
d
Young-of-the-year progeny.
e
Possessed large open ulcer across left lateral line.
b
268
G. H. Copp, K. J. Wesley and L. Vilizzi
Fig. 2. Length–frequency distributions of goldfish varieties captured
during March–May 2003 in ponds of Epping Forest (Essex, England)
and for introduced natives DRoad and DPond (Fig. 3, Table 4).
The pair-wise relationships of DPond, DPath and DRoad are
considered here graphically (Fig. 3) by virtue of their sociobiological interest (Yoccoz, 1991). With regard to adjusted
richness (S¢), pond area was the most influential geographical
variable for all three variety groups (Table 4), accompanied by
DPond and DRoad for non-native varieties, by vegetation cover
for goldfish varieties. Species–area relationships differed
among non-native, goldfish and introduced native varieties
(ARSS test: P < 0.001). Richness increased with pond area
more markedly in non-native, and less so in goldfish and
introduced native varieties, in this order (Fig. 4, Table 5).
When adjusted richness is considered, only the relationship for
non-native species was sound, this differing among non-native,
goldfish and introduced native varieties (ARSS test:
P < 0.001).
Relationships between fish densities and geographical variables were never statistically significant (Table 6), although
the density of goldfish is weakly related to DRoad (robust MM
multiple regression, P ¼ 0.104). The multiple regression
relationships between the rate of introductions (DSE) and
geographical variables were significant for DSE (P ¼ 0.07), in
particular vegetation cover (P ¼ 0.08) and DRoad (P ¼ 0.07),
with these relationships of greater statistical significance for
log10 + 1 transformed DSE (P ¼ 0.02), in particular pond
area (P ¼ 0.06) and DRoad (P ¼ 0.02). The bivariate relationship DSE and DRoad was significant (Fig. 5) and correspondingly this improved with DSE log10 + 1 transformed
(F ¼ 14.44, r2 ¼ 0.49, P ¼ 0.002). Also significant, but
again with a caveat for small sample size, were the bivariate
relationships between DSE and vegetated area (AV) was
significant (DSE ¼ )0.03AV + 2.41r2 ¼ 0.25, F ¼ 4.97,
P ¼ 0.042) as was that between DSE and DPath (DSE ¼
)2.36DPath + 3.11r2 ¼ 0.35, F ¼ 7.95, P ¼ 0.013). The
relationship between DRoad and adjusted variety richness
(DSE0 ) was also significant, but at a lower significance level
(DSE0 ¼ )1.94 log10 DR + 3.55,
r2 ¼ 0.30,
F ¼ 6.46,
P ¼ 0.023). Potential differences appear to exist between
young (restored <1.5 years ago) and older (restored
>2.5 years ago) ponds in the relationship between DSE and
DRoad (Fig. 5). For example, and with caveats for small sample
sizes, the relationship for young ponds approaches statistical
significance (SE ¼ )5.20x + 8.05, r2 ¼ 0.96, F ¼ 24.00,
Table 3
Exact unconditional independence test results for observed and expected (in brackets) frequencies of non-native, goldfish and introduced native
varieties of freshwater fishes captured in 17 restored ponds of Epping Forest (Essex, England), and of non-native and native varieties from
Wheeler’s (1998) data. Significant (a ¼ 0.10) associations in bold
Present study
Variable
Area
Small
Large
Cover
Sparse
Dense
DPond
Close
Far
DPath
Close
Far
DRoad
Close
Far
DHouses
Close
Far
Wheeler
Non-natives
Goldfish
Introduced natives
Non-natives
Absent Present P
Absent Present P
Absent Present P
Absent Present
Natives
P
Absent Present
P
6 (5.2)
2 (2.8)
5 (5.8)
4 (3.2)
7 (6.5)
0.527 3 (3.5)
4 (4.5)
3 (2.5)
8 (7.1)
0.622 3 (3.9)
3 (3.9)
3 (2.1)
–
0.484 –
–
–
–
–
–
–
–
–
2 (3.3)
6 (4.7)
5 (3.7)
4 (5.3)
3 (4.1)
0.262 7 (5.9)
4 (2.9)
3 (4.1)
4 (4.5)
0.321 7 (6.5)
3 (2.5)
3 (3.5)
–
0.622 –
–
–
–
–
–
–
–
–
5 (3.8)
3 (4.2)
3 (4.2)
6 (4.8)
5 (4.7)
0.302 5 (5.3)
3 (3.3)
4 (3.7)
7 (5.2)
1.000 4 (5.8)
1 (2.8)
5 (3.2)
–
0.082 –
–
–
–
–
–
–
–
–
2 (3.8)
6 (4.2)
6 (4.2)
3 (4.8)
3 (4.7)
0.121 7 (5.3)
5 (3.3)
2 (3.7)
4 (5.2)
0.121 7 (5.8)
4 (2.8)
2 (3.2)
–
0.262 –
–
–
–
–
–
–
1 (4.2)
7 (3.8)
8 (4.8)
1 (4.2)
3 (5.3)
0.002 7 (4.7)
6 (3.7)
1 (3.3)
3 (5.8)
0.034 8 (5.2)
6 (3.2)
0 (2.8)
2 (4.1)
0.005 5 (2.9)
19 (16.9)
0 (0.6)
10 (12.1) 0.077 1 (0.4)
21 (20.4)
14 (14.6) 0.320
2 (4.2)
6 (3.8)
7 (4.8)
2 (4.2)
3 (5.3)
0.041 7 (4.7)
6 (3.7)
1 (3.3)
4 (5.8)
0.034 7 (5.2)
5 (3.2)
1 (2.8)
2 (3.7)
0.082 5 (3.3)
17 (15.3)
0 (0.5)
12 (13.7) 0.167 1 (0.5)
19 (18.5)
16 (16.5) 0.391
–
–
Introduction of ornamental fish into ponds
269
Fig. 3. Surface plots for pair-wise multiple Poisson regression relationships between richness and distance from pond, road, and path for
unexpected native, non-native, and goldfish varieties of freshwater fishes captured in 17 restored ponds of Epping Forest (Essex, England).
Shaded plots are for significant relationships at P ¼ 0.10, white plots at P < 0.20 (shown for consistency) (see also Table 4)
P ¼ 0.128) whereas that for older ponds is highly significant
(SE ¼ )0.35x + 0.67, r2 ¼ 0.60, F ¼ 17.90, P < 0.002).
The progressive change in the relative abundance, species
richness (and adjusted species richness) of non-native varieties
of fish in Epping Forest ponds during the 1990s, summarized
by the exotic-ness and Jaccard’s ratios (Fig. 6d), reveals an
increasing influence, during the last decade, of non-native
fishes, which exert a homogenizing effect on fish community
composition (Jaccard’s ratio) at the species level but a
differentiating effect when species variety is considered. The
rise in non-native species influence is corroborated in the EUIT
on Wheeler’s (1998) data, with only one significant deviation
from random (Table 3): DRoad for non-native varieties
(P ¼ 0.08), which was of much lower statistical significance
than that for our data. When time intervals (1992–1994, 1995–
1996, 1997–1998) within Wheeler’s (1998) data set were
examined separately, the only statistically significant deviation
from expected was with regard to DHouses for non-native
varieties, which occurred more often than expected in ponds
close to roads (P ¼ 0.032) during the most recent interval
(1997–1998). Similarly, and with a caveat for small sample size,
only one significant regression relationship was observed, for
1995–1996 with regard to variety richness, which decreased in
introduced native varieties with increasing DRoad (slope ¼
)0.004, SE ¼ 0.002, t ¼ )1.730, d.f. ¼ 1, deviance
¼ 3.411, residual d.f. ¼ 12, residual deviance ¼ 11.152,
P ¼ 0.065).
Repeated sampling at Jubilee Pond, once in spring and then
once after each of three summer fairs (held on open ground
near the pond) provided evidence of fair-ground prizes and
garden-pond fish being abandoned (Table 2, Fig. 7). In spring,
prior to the first fair held near Jubilee Pond since its
construction, no fish were captured despite intensive sampling.
Following the first summer fair, two golden goldfish of size
consistent with goldfish being given away as prizes
(D. Huckfield, personal communication) were captured at
the end of this long, narrow pond nearest the fair ground.
Whereas, fish from a garden pond were captured at the end of
the pond adjacent to a car park – the presence of these fish
corroborated a report received by a Forest Keeper that a
person had recently been observed releasing large fish into the
pond (D. Huckfield, pers. comm.). Sampling after the second
summer fair was delayed because of illness, and no goldfish of
size consistent with fairground prizes were found, but a lion’s
head goldfish was captured, suggesting a subsequent release of
aquarium/garden pond fish. A large number of young-of-theyear brown goldfish of various sizes were also observed on
24 July, suggesting two sub-cohorts (spawnings). Sampling
soon after the third (and last) summer fair, yielded about a
dozen goldfish of size consistent with fair-ground prizes as well
as a large number of brown goldfish of three or four
sub-cohorts (spawning events).
Discussion
The distribution of fish in restored Epping Forest ponds was
not random and can be attributed to human access routes
(Table 3), in particular distance from the nearest road (Figs 3
and 4) for both non-native varieties and unexpected native
species. For example, the sequence of occurrence and sizedistributions of non-native fishes observed in Jubilee Pond
evinces the abandonment of unwanted fish (from garden ponds
and fairground prizes) and their immediate reproduction
(Table 2, Figs 2 and 7). This was particularly true of goldfish,
which are known to undertake multiple spawning events,
especially following translocation, during the same vegetative
season (e.g. Gillet et al., 1977). The successful establishment of
goldfish in restored ponds is probably facilitated by the genetic
diversity that comes with sporadic, unauthorized introductions
of fish derived from a variety of sources (Sakai et al., 2001).
Our sampling may have underestimated the numbers of ÔredÕ
goldfish abandoned in public ponds. These brightly pigmented
270
G. H. Copp, K. J. Wesley and L. Vilizzi
Table 4
Poisson multiple regression models for richness (S) and robust MM multiple regression models for adjusted richness (S¢) of introduced native,
non-native and goldfish varieties of freshwater fishes captured in 17 restored ponds of Epping Forest (Essex, England), and of native and nonnative varieties from Wheeler’s (1998) data as a function of geographical features (Table 1). Significant (a ¼ 0.10) probabilities (chi-square) in
bold. Value ¼ intercept or slope value for the variable considered (see also Fig. 3)
Richness
Adjusted richness
Parameters
Variable
Value SE
Present study
Non-natives
Intercept 2.315
Area
0.001
Cover
)0.012
)0.001
DPond
0.162
DPath
)0.242
DRoad
0.003
DHouses
Goldfish
Intercept 0.978
Area
)0.001
Cover
)0.008
0.001
DPond
0.320
DPath
)0.329
DRoad
0.001
DHouses
Introduced natives
Intercept )0.501
Area
0.001
Cover
)0.001
0.002
DPond
0.145
DPath
)0.242
DRoad
0.004
DHouses
Wheeler
Non-natives
Intercept 0.357
0.001
DRoad
DHouses )0.001
Natives
Intercept 1.434
)0.003
DRoad
DHouses )0.001
t
Analysis of deviance
Parameters
d.f. Deviance Resid. d.f. Resid. deviance P
Value SE
Wald test
Chi-square d.f. Wald
t
P
0.745 3.106 1
0.001 0.432 1
0.008 )1.312 1
0.002 )0.886 1
0.162 1.000 1
0.220 )1.097 1
0.004 0.774 1
1.393
1.939
2.243
9.453
21.220
1.225
16
15
14
13
12
11
10
39.308
37.915
1.834
35.672
26.218
4.999
3.773
0.252 0.330 0.763 1
0.238 0.001 0.001 22.062 1
0.164 )0.001 0.004 )0.305 1
0.134 )0.001 0.001 )0.549 1
0.002 0.007 0.010 0.706 1
<0.001 )0.006 0.002 )3.563 1
0.268 0.001 0.001 0.566 1
0.927 1.056 1
0.001 )0.426 1
0.010 )0.783 1
0.002 0.532 1
0.227 1.412 1
0.278 )1.223 1
0.006 0.106 1
0.019
0.651
2.986
3.610
17.847
0.085
16
15
14
13
12
11
10
26.937
26.919
1.738
23.933
20.322
2.475
2.390
0.891
0.420
0.084
0.057
<0.001
0.771
1.577 )0.318
0.001 0.364 1
0.016 )0.044 1
0.004 0.565 1
0.263 0.552 1
0.352 )0.686 1
0.007 0.611 1
0.941
0.002
3.607
1.782
3.528
0.805
16
15
14
13
12
11
10
15.195
14.253
4.529
10.646
8.864
5.336
4.531
)0.073 0.040 )1.827 1
0.332 0.001 0.001 5.372 1
0.965 0.001 0.001 1.600 1
0.057 0.001 0.001 1.620 1
0.182 )0.001 0.001 )1.433 1
0.060 0.001 0.001 0.963 1
0.370 0.001 0.001 1.478 1
0.187 1.192 1
0.002 0.020 1
0.001 )0.295 1
0.001
0.089
35
34
33
33.012
33.012
32.923
0.989
0.765
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
0.116 12.389 1
0.001 )1.934 1
0.001 )0.357 1
5.014
0.130
35
34
33
43.429
38.415
38.284
0.025
0.718
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
0.162
0.001
)0.001
)0.001
0.001
)0.001
)0.001
0.073
0.001
0.001
0.001
0.002
0.001
0.001
2.215
)1.958
)1.650
)0.503
0.414
)1.714
)1.033
1
1
1
1
1
1
1
244.711 <0.001
0.982
0.382
3.796
0.051
0.190
0.663
5.543
0.018
1.305
0.253
3.834
2.723
0.253
0.171
2.937
1.067
0.050
0.099
0.615
0.679
0.087
0.302
28.854 <0.001
2.560
0.110
2.626
0.105
2.052
0.152
0.927
0.336
2.183
0.139
Table 5
Species–area relationships for non-native, goldfish and introduced
native varieties of freshwater fishes captured in 17 restored ponds of
Epping Forest (Essex, England). Values (± ASE) for the parameters
(c, z) are reported (see also Fig. 4)
Statistic
Raw richness
n
17
c
0.417
z
0.185
0.541
r2
Adjusted richness
n
17
c
0.013
z
0.599
2
0.737
r
Fig. 4. Linear relationship of the rate of introduction (number of
varieties per year: DSE) of non-native fishes introduced into ponds of
Epping Forest (Essex, England)
Goldfish
Introduced
natives
± 0.402
± 0.108
17
0.323 ± 0.339
0.142 ± 0.123
0.442
17
0.089 ± 0.108
0.221 ± 0.131
0.472
± 0.021
± 0.156
17
0.073 ± 0.200
0.335 ± 0.277
0.234
17
0.737 ± 1.414
0.086 ± 0.241
0.152
Non-natives
goldfish are more visible to avian predators (Ödeen and
Håstad, 2003) and thus are less likely than the brown variety to
survive in ponds subjected to grey heron predation. Grey
herons were observed fishing on numerous occasions during
our field work, and they are known to predate on the most
abundant available prey (Adams and Mitchell, 1995), with
Introduction of ornamental fish into ponds
271
Table 6
Robust multinomial model MM multiple regression models for the
density of non-native, goldfish and introduced native varieties of
freshwater fishes captured in 17 restored ponds of Epping Forest
(Essex, England) as a function of geographical features (Table 1).
Biologically interesting probabilities in bold
6.0
5.0
Non-natives
Intercept
2.700
Area
0.001
)0.003
DPond
0.020
DPath
)0.007
DRoad
)0.001
DHouses
Cover
)0.018
Goldfish
Intercept
1.848
Area
0.001
)0.002
DPond
0.022
DPath
)0.005
DRoad
)0.001
DHouses
Cover
)0.013
Introduced natives
Intercept
0.068
Area
0.001
0.001
DPond
0.001
DPath
)0.001
DRoad
)0.001
DHouses
Cover
)0.001
SE
t-test
v2 d.f.
Wald
P
2.447
0.001
0.004
0.058
0.010
0.003
0.031
1.103
)0.474
)0.693
0.351
)0.725
)0.375
)0.583
1
1
1
1
1
1
1
0.816
0.001
0.001
0.019
0.003
0.001
0.010
2.266
)1.131
)1.454
1.118
)1.623
)0.832
)1.313
1
1
1
1
1
1
1
1.280
2.114
1.250
2.634
0.692
1.725
0.258
0.146
0.263
0.104
0.406
0.189
0.063
0.000
0.001
0.001
0.001
0.001
0.001
1.073
)0.691
0.017
0.357
)0.663
)0.592
)0.488
1
1
1
1
1
1
1
0.479
0.001
0.128
0.440
0.351
0.238
0.489
0.987
0.721
0.507
0.554
0.625
0.224
0.480
0.123
0.526
0.141
0.339
Non-natives
3.0
2.0
0.636
0.488
0.726
0.468
0.707
0.560
Goldfish
1.0
Unexpected natives
0.0
Non-natives
10.0
Adjusted richness
Value
Richness
4.0
Variable
8.0
6.0
4.0
Goldfish
2.0
Unexpected natives
0.0
10
100
1000
10 000
100 000
Area
clear size selectivity (Britton and Moser, 1982) as well as
elevated violet sensitivity (e.g. Ödeen and Håstad, 2003); this
suggests that more colourful prey items (golden/red goldfish)
are taken preferentially over more cryptic prey (e.g. brown
goldfish). This said, goldfish would be expected to benefit from
greater amounts of aquatic vegetation cover, but goldfish
densities were not correlated with percentage cover and the
number of goldfish varieties decreased with increasing percentage cover.
Wheeler’s (1998) assumption that ponds close to roads, car
parks and fairgrounds are likely sites for the introduction of
non-native fishes (and in particular goldfish) was validated, at
least for ponds of Epping Forest. This was particularly true of
Jubilee Pond for which we were able to obtain time-series
information on introductions (Table 2, Fig. 7). Our results
contribute to growing evidence on the role of roads as
transport routes for the dispersal of non-native species
(Trombulak and Frissell, 2000). Humans are indeed the main
active agents in the dispersal of ornamental fishes in ponds of
Epping Forest (Table 2, Fig. 3). The highly significant relationships between the number (SE) of non-native varieties and
distances from nearest road and footpath suggest an active
role. Indeed, the rate at which these introductions takes place
appears to be about 3.5 varieties per year in new or recently
restored ponds if distance from road is used as the estimator
(Figs 4 and 5). The causative role of humans is further
corroborated by the relationship between SE0 and distance to
nearest house. Percentage area of pond occupied by aquatic
vegetation and distance to nearest house both predict a much
lower introduction rate (about one variety per 2 years), but
distance from nearest road is statistically a far more reliable
estimator. A similar causal relationship between roads and
non-native plants species has recently been described, with the
richness and the area covered by exotic plants being >50%
Fig. 5. Species–area relationships for the variety richness (upper
graph) and fish density-adjusted variety richness (lower graph) of
fishes captured during 2003 in 17 restored ponds of Epping Forest
(Essex, England). Separate curves for non-native (dotted line, open
circles), goldfish (dashed line, grey circles) and unintentional
(i.e. unexpected) native (solid line, filled circles) varieties are provided.
Overlap in data points for non-native and goldfish varieties is
highlighted by slight displacement (see also Table 5)
greater, and the richness of native species 30% lower, at 50 m
distances from paved roads when compared with four-wheel
track routes, and the verges along paved roads tended to have
greater cover of common exotic forb species (Gelbard and
Belnap, 2003).
The relationships between distance from road and ornamental fish richness may also be valid in other areas of the
British Isles, but this remains to be tested. The temporal trend
in the composition of fishes in Epping Forest ponds (Fig. 6)
indicates an increasing predominance of non-native fish species
and varieties thereof. In the first two periods of Wheeler’s
(1998) study, goldfish and common carp were the only nonnative species reported, and they played a homogenizing role
(Fig. 6d) except during 1995–1996 and 1997–1998, when the
arrival of topmouth gudeon plays a differentiating role
(McKinney, 2004). However, when all varieties of non-native
fish are considered, they definitely serve to differentiate
between the time periods as regards the fish community
composition. The increasingly important role of non-native
fishes can be attributed to changes in society’s attitude and
behaviour with regard to ornamental fishes. The abandonment
(or donation) of goldfish to ponds is not a recent phenomenon
(e.g. West, 1910), but the incidence of non-native introductions
appears to have risen substantially in the last decade (Fig. 6).
This is most apparent in the latter phase (1997–1998) of
272
G. H. Copp, K. J. Wesley and L. Vilizzi
Fig. 7. Length–frequency distributions of goldfish varieties captured
from Jubilee Pond (Essex) on consecutive sampling dates (bottom to
top) following bank-holiday fairs held adjacent to the pond (Table 2).
Goldfish of size consistent with those given away as fair-ground prizes
are given as black bars, whereas the lone specimen of the lion’s head
variety is given as a striped bar
Fig. 6. For three time intervals of Wheeler’s (1998) data (1992–1994,
1995–1996, 1997–1998) and for our data from 2003 from ponds of
Epping Forest (Essex, England), illustrated are (a) the proportions of
native and non-native species/varieties, (b) the variety richness
0
) and non-native varieties (SE0 ),
(number of varieties) for native (SN
(c) the adjusted variety richness (S¢) and (d) the exoticness index
0
) and the ratio of Jaccard’s coefficient of similarity (JCSE/
(IE ¼ SE0 =SN
JCSN) at the species (filled circles) and variety (open circles) levels
Wheeler’s study period, when the association between distance
from road and the incidence of non-native varieties was first
observed (see Results).
Taken as a whole, the relationships between variety richness,
access proximity and pond area in our data suggest that ponds
are selected (by the general public) for the introduction of fish
according two main factors: proximity and size. Ponds within
about 10 m of a road or footpath are most likely to receive
both non-native and native varieties, whereas larger ponds are
more likely to sustain a wider diversity of both non-native and
native varieties. Therefore, one might speculate that the
primary motivations for the release of fish into public ponds
near access routes are related to personal beliefs (ethnicity,
animal protection) for smaller water bodies and to angling
amenity for larger water bodies, with a caveat for the potential
influence of grey heron predation on fish assemblage structure.
The goldfish has become more and more commonplace in
the aquarium and garden trade, and its intrinsic economic
value has subsequently declined. This ready availability of
goldfish in the ornamental trade equates to an elevated
Ôfrequency of occurrence in natureÕ, an intrinsic dispersal
property of reproductive bodies as regards pond colonization
(Talling, 1951). With the increasing affluence of British society
in the late 20th century, the pressure on threatened species is
expected to increase (Naidoo and Adamowicz, 2001) as the
importance of introduced non-native species increases (Fig. 6).
The range of unusual fish species/varieties available in the
ornamental trade has dramatically increased, and goldfish are
now so common that the species is viewed by some members of
the general public, albeit incorrectly, as indigenous to the UK
and therefore of no apparent threat to native species. This
misconception is perhaps facilitated by the species legal status
as Ôordinarily residentÕ under UK legislation.
Cultural beliefs and practices are clearly a motivation for
some introductions. For example, Crossman and Cudmore
(1999) attributed the release of some non-native fishes into
open waters (of Ontario, Canada) to the ancient Chinese
practice, endorsed by the Buddhist faith, of releasing a live fish
as a highly approvable act of compassion, a Ôgood deedÕ to
accumulate merits for favourable judgement in the afterlife.
Such releases of live ornamental fishes to Epping Forest ponds
are accompanied by the provision of food, which is manifest
by bags of rice and other ÔfastÕ foods found at pond’s edge
(G.H. Copp and K.J. Wesley, pers. obs.). This practice is
linked to cultural/religious beliefs, i.e. the reincarnate souls of
deceased relatives are embodied in lower animals – so the
introduction of foodstuffs to the ponds is de facto the provision
for deceased family members. These introduced foodstuffs
constitute a major injection of nutrients to ponds, which are
already subjected to an elevated nutrient load (land runoff,
anglersÕ ground bait, etc.), and this accelerates eutrophication.
Introductions of fish to ponds by humans do not appear
restricted to non-native ornamental fish varieties, as the
number of native species/varieties (SN) also increases significantly with decreasing pond distance from the nearest road
(Fig. 3, Appendix 1). This may be expected, given the highly
managed nature of these artificial ponds and the practice of
(illegally) introducing native fish species (e.g. rudd, tench,
roach Rutilus rutilus), or their ornamental (golden rudd,
golden tench) varieties, into still waters for sport fishing
Introduction of ornamental fish into ponds
(e.g. Trombulak and Frissell, 2000). In the light of the
increasing prevalence of non-native fishes, especially goldfish,
in public ponds (Table 2, Fig. 7), the implications of our
findings for management and policy are threefold: (i) the use of
ornamental fishes (in particular goldfish) as fairground prizes
should be re-evaluated, with a view to restriction (in the UK,
this restriction has effectively come into force during 2004
under animal protection legislation, which includes prohibition
of the use of goldfish as fairground prizes); (ii) efforts to
protect and conserve the genetic integrity of crucian carp
populations should concentrate on ponds that are situated at
greater distances from public access routes (roads, pathways,
car parks, fair ground sites) so as to enhance the chances of
maintaining genetically pure self-sustaining populations; and
(iii) increased public awareness (i.e. risk communication)
should be stimulated through educational programmes that
explain and highlight the potential and real risks of non-native
species to our native flora and fauna, such as the genetic
impact of goldfish on crucian carp (Wheeler, 2000; Tóth et al.,
2005).
Acknowledgements
This study was funded jointly by the UK Department of
Environment, Food & Rural Affairs (Defra) and the Corporation of London. We are especially grateful to P. Broxup, D.
Huckfield and P. Murfin for assistance in the field and
historical information on the ponds, to J. Dagley and T.
Moxey for background information on the ponds, and to R.
Bush, D. Goldsmith, M. Ives and W. Riley for assistance in the
laboratory.
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Author’s address: Gordon H. Copp, Salmon & Freshwater Team,
Centre for Environment, Fisheries & Aquaculture
Science (CEFAS), Pakefield Road, Lowestoft, Suffolk NR33 OHT, UK.
E-mail: [email protected]
Appendix 1
Poisson simple regression models for richness (S) of introduced native, non-native and goldfish varieties of freshwater fishes captured in 17
restored ponds of Epping Forest (Essex, England) as a function of sampling effort (Minutes) and fish density. Value ¼ intercept or slope value
for the variable considered. Significant (a ¼ 0.10) probabilities (v2) in bold
Parameters
Analysis of deviance
Variable
Value
SE
t-test
Non-natives
Intercept
Minutes
Intercept
Density
–1.085
0.022
)0.072
0.066
0.521
0.006
0.277
0.019
–2.083
3.726
)0.259
3.465
Goldfish
Intercept
Minutes
Intercept
Density
)1.407
0.018
)0.908
0.090
0.646
0.007
0.419
0.026
–2.176
2.476
)2.165
3.478
Introduced natives
Intercept
)2.298
Minutes
0.020
Intercept
)1.351
Density
0.105
0.966
0.011
0.505
0.046
)2.378
1.926
)2.674
2.274
d.f.
Deviance
1
16.158
1
10.765
1
6.483
1
11.647
1
4.265
1
4.204
Resid. d.f.
Resid. deviance
16
15
16
15
39.308
23.149
39.308
28.543
16
15
16
15
26.937
20.094
26.937
15.290
16
15
16
15
15.195
10.930
15.195
10.991
P
<0.001
0.001
0.009
<0.001
0.039
0.040