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ORIGINAL PAPER
Source–sink dynamics explain the distributionand persistence of an invasive population of common carpacross a model Midwestern watershed
Justine D. Dauphinais . Loren M. Miller . Reid G. Swanson . Peter W. Sorensen
Received: 27 July 2017 / Accepted: 15 January 2018
� Springer International Publishing AG, part of Springer Nature 2018
Abstract Source–sink theory is an ecological frame-
work that describes how site and habitat-specific demo-
graphic rates and patch connectivity can explain
population structure and persistence across heteroge-
neous landscapes. Although commonly used in conser-
vation planning, source–sink theory has rarely been
applied to the management of invasive species. This
study tested whether the common carp, one of the
world’s most invasive species, exhibits source–sink
dynamics in a representative watershed in the Upper
Mississippi River Basin comprised of a dozen intercon-
nected ponds and lakes. To test for source–sink popu-
lation structure, we used standard fish sampling
techniques, tagging, and genetic assignment methods
to describe habitat-specific recruitment rates and disper-
sal. Five years of sampling revealed that while adult carp
were found across the entire watershed, reproductive
success (the presence of young carp) was restricted to
shallow ponds. Additionally, nearly a third of the carp
tagged in a representative pond dispersed into the
connected deeper lakes, suggesting that ponds in this
system serve as sources and lakes as sinks. This
possibility was confirmed by microsatellite analysis of
carp tissue samples (n = 1041) which revealed the
presence of two distinct strains of carp cohabitating in the
lakes, whose natal origins could be traced back to one of
two pond systems, with many adult carp attempting to
migrate back into these natal ponds to spawn. We
conclude that the distribution and persistence of invasive
carp in complex interconnected systems may often be
driven by source–sink dynamics and that their popula-
tions could be controlled by suppressing reproduction in
source habitats or by disrupting dispersal pathways,
instead of culling individuals from sink habitats.
Keywords Demographics � Microsatellite �Homing � Aquatic invasive species � Habitat
heterogeneity � Watershed scale
Introduction
The proliferation of invasive fishes is a growing
problem that poses serious threats to the integrity of
aquatic ecosystems around the world (Kolar and
Electronic supplementary material The online version ofthis article (https://doi.org/10.1007/s10530-018-1670-y) con-tains supplementary material, which is available to authorizedusers.
J. D. Dauphinais � L. M. Miller � R. G. Swanson �P. W. Sorensen (&)
Department of Fisheries, Wildlife, and Conservation
Biology, University of Minnesota, 135 Skok Hall, 2003
Upper Buford Circle, Saint Paul, MN 55108, USA
e-mail: [email protected]
J. D. Dauphinais
e-mail: [email protected]
L. M. Miller
Minnesota Department of Natural Resources, 135 Skok
Hall, 2003 Upper Buford Circle, Saint Paul, MN 55108,
USA
123
Biol Invasions
https://doi.org/10.1007/s10530-018-1670-y
Lodge 2002; Garcıa-Berthou et al. 2005; Vitule et al.
2009). Successful control of invasive populations
requires a detailed understanding of the drivers of
population structure and demography across relevant
spatial and temporal scales (Travis and Park 2004).
Understanding population dynamics is challenging in
complex freshwater systems, especially networks of
drainage lakes and large rivers that are often charac-
terized by high levels of habitat heterogeneity and
connectivity. Source–sink theory, a well-established
ecological framework, describes how dispersal of
organisms between patches of varying habitat quality,
some of which can support local population growth and
others which cannot, can drive overall population
persistence at a landscape scale (Pulliam 1988; Dias
1996; Dunning et al. 1992). In source–sink theory,
habitat patches that support local population growth
and serve as net exporters of individuals are known as
‘‘sources’’, while habitat patches where mortality
exceeds natality and thus cannot sustain local popula-
tions are known as ‘‘sinks’’ (Dias 1996). Because local
populations in sink habitats tend towards extinction
without an influx of recruits, dispersal from sources to
sinks is both necessary for, and explains, overall
metapopulation persistence (Figueira and Crowder
2006). Recent studies have expanded this conceptual
framework and it is now accepted that source–sink
dynamics may be driven by multiple mechanisms that
result in habitat-specific demographic rates such as
patchily distributed predators (Woodford and McIn-
tosh 2010), variable harvest rates (Novaro et al. 2005),
or varying susceptibility of habitat patches to environ-
mental catastrophes or instability (Thomas et al. 1996;
Frouz and Kindlmann 2001).
Source–sink theory is frequently used in conserva-
tion planning to understand and manage the viability
(probability of persistence) of various populations at a
landscape scale (Margules and Pressey 2000; Carroll
et al. 2003; Sarkar et al. 2006). For example, in aquatic
systems, the source–sink framework has been used to
inform the locations of marine protected areas
(Roberts 1998; Crowder et al. 2000), to evaluate the
consequences of commercial harvest policies (Wil-
berg et al. 2008), and to model the viability of
vulnerable fish populations (Woodford and McIntosh
2010; Fullerton et al. 2016). Despite the many
applications of source–sink theory to the management
of rare, vulnerable, or commercially important aquatic
species, it has rarely been applied to the control of
invasive species although the utility of this approach
has been suggested and modeled (Shea 1998; Travis
and Park 2004; Brown and Gilligan 2014). If a source–
sink framework could accurately describe the demog-
raphy of an invasive population, then it could be used
to elucidate the extent to which different habitat
patches contribute to overall population growth and
persistence, and thus how various management strate-
gies might be implemented to control that species. For
example, if an invasive fish population exhibited
source–sink dynamics, management strategies such as
altering source habitats to reduce reproductive success
or preventing dispersal between source and sink
habitat patches might be implemented to reduce the
viability or size of the population.
Empirical evidence of source–sink dynamics in
natural systems, and in aquatic systems in particular, is
rare because of difficulties associated with measuring
both demographic rates and dispersal patterns across
large spatial scales (Diffendorfer 1998; Runge et al.
2006; Furrer and Pasinelli 2015). The common carp
(Cyprinus carpio), a large cyprinid native to Eurasia
(Kohlmann and Kersten 2013), is as an excellent
model to investigate source–sink dynamics in an
invasive fish because it often inhabits complex
heterogeneous systems with varying levels of connec-
tivity and reproductive habitat quality (Balon 1995;
Brown et al. 2005; Sorensen and Bajer 2011). This
species (hereafter ‘‘carp’’) has invaded millions of
hectares of interconnected lakes, rivers, and wetlands
across the world and is considered one of the most
pervasive and damaging invasive fishes (Lowe et al.
2000; Weber and Brown 2009; Zambrano et al. 2006),
highlighting the need for innovative management
strategies that exploit its life history attributes.
Intriguingly, newly emerging evidence suggests that
adult carp frequently exhibit a strategy known as
partial migration (Bajer et al. 2015b; Chizinski et al.
2016), in which only a portion of a population
migrates (Jonsson and Jonsson 1993). In the case of
adult carp in the Upper Mississippi River Basin, it
appears that 10–50% of their populations routinely
migrate each spring to reproduce in adjoining portions
of watersheds, with the remaining residents spawning
in place (Bajer et al. 2015b; Chizinski et al. 2016). It
has been hypothesized that this life history strategy
allows migratory carp to maximize reproductive
success by taking advantage of spawning habitats that
occasionally lack predators because of environmental
J. D. Dauphinais et al.
123
instability (Bajer and Sorensen 2010), while non-
migratory individuals experience higher survival
rates, but lower reproductive output (Bajer et al.
2015b). This life history strategy results in spatially
explicit demographic rates and lends itself to further
investigation under the source–sink framework.
There is circumstantial evidence that some inva-
sive populations of carp may exhibit source–sink
dynamics in a variety of freshwater systems. Recent
studies have shown that select shallow nursery habitats
contain the vast majority of young carp and likely
contribute disproportionately to carp recruitment suc-
cess in both riverine systems of Australia (Driver et al.
2005; Stuart and Jones 2006; Crook et al. 2013) and in
many networks of drainage lakes in the Upper
Mississippi River Basin (Bajer and Sorensen 2010;
Bajer et al. 2012; Silbernagel and Sorensen 2013). In
fact, in central Minnesota, despite high propagule
pressure across entire watersheds, carp reproductive
success is seemingly restricted to connected shallow
ponds characterized by low winter-time oxygen levels
and a low abundance of egg- and larval predators that
are intolerant of hypoxia (Bajer and Sorensen 2010;
Bajer et al. 2012; Silbernagel and Sorensen 2013).
Specifically, carp age structure data from several
distinct watersheds indicates that carp recruitment is
notably more successful in years following harsh
winters (Bajer and Sorensen 2010). The authors
speculate that this pattern was due to a lack of
predators in adjoining select shallow basins prone to
intermittent winterkill. Subsequent studies support
this hypothesis with evidence that young carp are only
found in water bodies that lack abundant native
micropredators (Bajer et al. 2012) and that over 95%
of naturally spawned carp eggs in normoxic lakes
disappear before hatching while large numbers of carp
eggs are simultaneously consumed by bluegill sunfish,
Lepomis macrochirus, a native micropredator (Silber-
nagel and Sorensen 2013). Direct evidence that young
carp disperse from these presumptive recruitment
‘‘hotspots’’ to putative sink habitats is presently
lacking. The possibility that this life history strategy
might be consistent with source–sink theory has not
yet been examined.
In this study, we collected and then used spatially
explicit demographic data coupled with information
on movement patterns of tagged individuals to test the
hypothesis that a population of common carp exhibits
source–sink dynamics in a typical system of
interconnected lakes and ponds in the headwaters of
the Upper Mississippi River Basin. First, we tested
whether the relative abundance of carp in their first
year of life (young-of-year, YOY) differed between
discrete habitat patches (lakes and ponds), with some
habitats producing a surplus of individuals (i.e.,
serving as putative sources) and some not producing
enough to sustain population growth (i.e., serving as
sinks). Second, we hypothesized that carp disperse
from putative sources to sinks at rates sufficient to
maintain the local populations in sink habitats. Third,
based on a preliminary finding of genetic structure in
this system, we hypothesized that the distribution of
genetically distinct strains of carp would reflect this
source–sink population structure across both space
and time. This study presents the first empirical
evidence that we are aware of for source–sink
dynamics regulating the persistence of an invasive
fish metapopulation and describes a novel control
strategy.
Methods
Study site
Our study took place in the Phalen Chain of Lakes
Watershed (hereafter, Phalen Watershed) located in
Ramsey County, Minnesota, USA (45�003000N,
93�303600W; Fig. 1). This system is very similar in
size and habitat complexity to many freshwater
systems in the previously glaciated regions of the
Upper Mississippi River Basin (as well as many other
interconnected temperate lake systems around the
world) and has served as a model to understand carp
ecology, migration, and population dynamics (Bajer
et al. 2011, 2012; Silbernagel and Sorensen 2013;
Chizinski et al. 2016). The Phalen Watershed drains
6100 hectares of urban land through a series of
interconnected lakes, shallow ponds, and creeks,
which eventually outflows to the Mississippi River.
The hydrology of the Phalen Watershed has been
altered by human development in the past century
including the draining of wetlands, ditching of creek
segments, construction of storm water ponds, and
installation of fish barriers to block passage from the
Mississippi River, all of which may affect the
distribution and abundance of carp. This system
contains four deep lakes (Surface area: 29–95 ha;
Source–sink dynamics explain the distribution and persistence of an invasive population
123
maximum depth: 3–28 m), which we term here ‘‘main
lakes’’, that are connected by navigable stream
channels and fed by two inflowing creeks, each of
which drains a series of four shallow ponds (maximum
depth \ 2 m), forming the Kohlman Creek and
Gervais Creek subwatersheds. A key feature that
distinguishes the lakes and ponds (i.e., different habi-
tat patches), aside from their depth and size, is their
susceptibility to winter hypoxia. Unlike the deeper
main lakes, the shallow ponds in this system experi-
ence periodic low winter oxygen levels and partial
winterkills and thus do not naturally support robust
native fish communities including the bluegill sunfish
(Osborne 2012), a known predator of carp eggs and
larvae (Bajer et al. 2012; Silbernagel and Sorensen
2013). The fish communities of the ponds are instead
dominated by species tolerant of hypoxia such as the
common carp, fathead minnow (Pimephales
Keller
Gervais
Kohlman Creeksubwatershed
Gervais Creek subwatershed
Kohlman
Phalen
N
CaseyMarkham
Upper Kohlman Basin
Willow
Interstate
Owasso Basin
MillSavage
Fig. 1 Map of the study sites in the Phalen Watershed (Ramsey
County, Minnesota, USA; 45�003000N, 93�303600W). Water flows
from north to south and eventually drains to the Mississippi
River through a grated outlet. Phalen, Keller, Gervais and
Kohlman lakes, the ‘‘main lakes’’, are relatively deep ([ 3 m),
do not experience winter hypoxia, and support diverse fish
communities. The other basins, ‘‘ponds’’, are shallower (\ 2 m)
and periodically experience winter hypoxia and partial win-
terkill of sensitive fish species
J. D. Dauphinais et al.
123
promelas), bullhead (Ameiurus spp.), and green sun-
fish (Lepomis cyanellus) (Osborne 2012). Carp pop-
ulation surveys have been conducted in this watershed
for nearly a decade and show that adult carp are
present throughout the system and abundance
approaches 30 individuals per hectare in all 4 main
lakes with similar numbers inhabiting the ponds
(Online Resource 1). Carp biomass exceeds 100 kg
per ha which is a value commonly associated with
severe ecosystem degradation (Sorensen and Bajer
2011; Bajer et al. 2016). Adult carp have been
observed spawning in all lakes and ponds in this
system (Osborne 2012; Silbernagel and Sorensen
2013) and a study by Chizinski et al. (2016) also
found that between 10 and 50% of adult carp from the
main lakes swim between the lakes each year with
some entering Kohlman Creek during the spawning
season.
Identifying putative sources, sinks, and patterns
of dispersal
To test the hypothesis that carp reproductive output
varied among different habitat patches in the Phalen
Watershed (lakes and ponds), with some high-quality
habitats supporting the production of surplus carp and
some low-quality habitats not supporting population
growth, we compared the relative abundance of YOY
carp in all bodies of water. We expected YOY carp to
be abundant in the shallow ponds that are known to lack
egg-predators and would thus represent high-quality
habitats for carp reproduction and absent or scarce in
the main lakes which support robust native fish
communities (Osborne 2012). Surveys for YOY carp
were conducted in all accessible lakes and ponds in the
watershed each August for 5 years from 2009 to 2013
using trap-nets, a passive sampling gear designed for
sampling littoral fishes which is commonly and
reliably used by fisheries biologists (Hubert 1996).
Relative abundance was measured as the catch-per-
unit-effort (CPUE = number per net night) of YOY
carp (total length less than 150 mm; Osborne 2012)
sampled during standardized surveys using 5 trap-nets
(13 mm square mesh, 10 m lead, 1.8 m 9 0.9 m
frame) set equidistantly and perpendicular to shore
for approximately 24 h. All carp were counted, mea-
sured, and released at the location of capture. Sampling
protocols followed University of Minnesota Institu-
tional Animal Care and Use Committee protocols.
Having established putative sources based on YOY
catch rates, we next tested if carp emigrated from
putative sources to connected waters by tagging carp
in a representative shallow pond (Markham Pond,
6.5 ha, maximum depth 1.8 m) and then regularly
monitoring this pond and the basin downstream
(Upper Kohlman Basin, 4.3 ha, maximum depth
2 m, Fig. 1) for marked carp. Markham Pond was
chosen as our study site because it typifies many carp
nurseries, consistently supports high densities of
young carp (Osborne 2012, this study), and has a
single outflowing creek by which fish can leave the
pond (and which we could monitor). Carp were
sampled by boat electrofishing (5–12 A, 80–150 V,
20% duty cycle, 120-pulse frequency) during the open
water seasons (May–November) of 2012 and 2013
approximately once every 2 weeks for a total of 23
times in each location. Boat electrofishing is com-
monly employed for sampling freshwater fishes
including carp (Bajer and Sorensen 2010). All carp
sampled were measured, implanted with individually-
coded 23 mm passive integrated transponder (PIT)
tags (Oregon RFID, Portland, Oregon), and released at
the point of capture. Because immature carp less than
150 mm in total length were not implanted with tags
due to their small body size, movement rates represent
age-1 and older carp. Emigration was quantified by
calculating the percentage of all recaptured carp
tagged in Markham Pond that were later sampled in
Upper Kohlman Basin, a waterbody approximately
0.75 km downstream, which other studies have shown
to serve as a conduit to the main lakes (J. Dauphinais
and R. Swanson, personal observations).
Confirming source–sink structure
across the watershed using genetics
To quantify nursery contribution and patterns of
dispersal at a watershed scale, we characterized the
genetic structure of carp subpopulations across the
Phalen Watershed. We hypothesized that some source
habitats might have distinguishable genetic strains that
could be tracked across space and time based on pilot
experiments (L. Miller, unpublished) which had
already shown that genetic strains of carp could be
identified in this system using microsatellite DNA
loci. We hypothesized that strain contributions might
change across space because of distance from source
habitats, and with time, because of construction of
Source–sink dynamics explain the distribution and persistence of an invasive population
123
storm water infrastructure starting in the 1970s
including the re-engineering of wetlands as retention
basins and the installation of culverts and water
control structures that could impact fish passage.
Finally, because we predicted a lack of reproductive
success in sink habitats, we hypothesized that the
genetic composition of carp sampled in sink habitats
would reflect that of one or more source habitats
instead of reflecting the product of adults observed
spawning in sink habitats.
Sample collection
We collected tissue samples (fin clips) from carp in
putative sources (shallow ponds) in both the Kohlman
Creek and Gervais Creek subwatersheds as well as
from each of the main lakes that do not experience
winter hypoxia (i.e., Lakes Kohlman, Gervais, Keller,
and Phalen) (Table 1). Tissue samples were collected
from all carp captured in each locale to serve as
representative samples of each subpopulation. Carp
were captured via boat electrofishing, seining, trap-
netting, and baited traps between February 2011 and
October 2013 and all tissue samples were stored in
95% ethanol. To elucidate possible trends in source
contribution across years, we also aged a random
subset of carp sampled from the main lakes in 2012
following established protocols for carp asteriscii
otoliths (Bajer and Sorensen 2010). Briefly, asteriscii
otoliths were extracted, sectioned, and read by three
independent observers using a compound light micro-
scope. Additionally, in 2013 we collected separate
samples during the spawning season (May–June) to
characterize the genetic structure of reproductively
active groups of carp in both source and sink habitats
to determine whether and how they might be con-
tributing to local subpopulations and the greater
metapopulation (Table 1). We expected that adults
spawning in sink habitats would not be contributing to
local populations, but that adults spawning in source
habitats would be (survival of young carp would be
high in these habitats due to lack of micropredators).
Adults in putative sink habitats were captured actively
spawning in the littoral areas of the main lakes via boat
electrofishing. Adults attempting to spawn in putative
source ponds were captured in Kohlman and Gervais
Creeks via backpack electrofishing at temporary fish
barriers while they were performing upstream migra-
tions from the main lakes.
Analysis of genetic variation and structure
Genetic variation at 12 microsatellite DNA loci
previously established for carp (Crooijmans et al.
1997; Yue et al. 2004) was assessed following the
procedures outlined by Miller et al. (2009) using
4 mm2 of fin tissue (details reported in Online
Resource 2). Genetic structuring of carp subpopula-
tions across the watershed was then assessed by
analyzing multilocus genotype data from all samples
Table 1 Location, sample size, and sample dates of common carp tissue samples collected across the Phalen Watershed for genetic
analyses
Location Site Habitat type Sample size Sample year(s)
Kohlman Creek subwatershed Casey Pond 93 2011
Markham Pond 39 2011, 2012
Upper Kohlman Basin Pond 77 2012, 2013
Gervais Creek subwatershed Interstate Pond 63 2013
Owasso Basin Pond 5 2013
Gervais Mill Pond 2 2013
Main chain of lakes Kohlman Lake 94 2012
Gervais Lake 347 2011, 2012, 2013
Keller Lake 52 2013
Phalen Lake 30 2012, 2013
Spawning groups Kohlman Creek 147 2013
Gervais Creek 52 2013
Main lakes 40 2013
J. D. Dauphinais et al.
123
using the Bayesian clustering method in STRUC-
TURE version 2.3.4 (Pritchard et al. 2000). This
approach estimates the number of genetically distinct
clusters (K) in the dataset using a Markhov chain
Monte Carlo algorithm with no a priori assumptions
about population membership. We executed the
algorithm with a burn-in of 50,000 followed by a run
length of 200,000 for five replications at each K value
ranging from 1 to 5. The most likely value of K was
determined based on the plateauing of -log P(X/K)
values and the Evanno delta K method (Evanno et al.
2005) implemented in STRUCTURE HARVESTER
(Earl and VonHoldt 2012). Because STRUCTURE
analysis supported K = 2 (see Results: Genetic vari-
ation and structure), we were then able to use the
program NEWHYBRIDS (Anderson and Thompson
2002) to classify individuals as members of each
genetically distinct cluster (or ‘‘strain’’) or hybrids
between strains. NEWHYBRIDS estimates the prob-
ability an individual is a member of one of two strains,
a first-generation hybrid between strains (F1), or a
second-generation hybrid (F2 = F1 9 F1; back-
cross = F1 9 pure strain). The program was run with
an 80,000 step burn-in followed by a 200,000 step run.
Three replicate runs were performed to assure con-
gruence of estimates. Because NEWHYBRIDS is
ineffective at distinguishing hybrid categories in the
absence of multiple diagnostic loci (Anderson and
Thompson 2002), we classified individuals as pure
strain if probabilities exceeded 0.90 for either strain
and as ‘‘hybrid’’ otherwise (i.e., the combined prob-
abilities for F1, F2 and backcrosses exceeded 0.90).
After classifying individual carp, we calculated the
proportion of individuals of each distinct genetic strain
or hybrid in representative samples from the main
lakes and shallow ponds. First, we evaluated all
samples from non-spawning periods. Samples from
lakes were evaluated individually and then combined
to represent all putative sink habitats. Samples from
the shallow ponds were combined within each
subwatershed, but the Kohlman Creek and Gervais
Creek subwatersheds were examined separately. We
then assessed whether the genetic composition of the
carp subpopulation in the main lakes was similar over
time by evaluating the genetic assignments of indi-
viduals of known ages. Finally, we analyzed the
genetic composition of reproductively mature carp
sampled in three locations (main lakes, Kohlman
Creek, and Gervais Creek) during the spawning season
and compared it to that of residents captured from the
same locations outside of the spawning season.
Results
Identifying putative sources, sinks, and patterns
of dispersal
Although adult carp were observed spawning in most
lakes and ponds during this study, carp reproductive
success differed markedly in lake habitats compared to
shallow pond habitats. During 5 years of intensive fall
sampling for YOY carp, no YOY carp were caught in
any of the 4 main lakes, while YOY carp were found in
7 of the 8 shallow ponds (Table 2). Catch rates varied
considerably by year and location. Specifically, YOY
carp were found in 3 of the 4 shallow ponds in the
Kohlman Creek subwatershed in each of the years
surveyed (mean CPUE across years = 5.0, 44.3, and
4.1 carp/net for Casey, Markham, and Upper Kohlman
Basin, respectively) while the fourth pond, Willow,
had YOY carp in 2009 and 2010 but then suffered a
complete winterkill and had no carp in 2011–2013.
Although sampling efforts were limited in the Gervais
Creek subwatershed, YOY carp were sampled at least
once in 3 of the 4 ponds (CPUE = 23.0, 6.3, and 1.0
for Interstate, Owasso Basin, and Gervais Mill,
respectively).
As predicted in our study of carp dispersal, a large
number of marked carp emigrated out of Markham
Pond, a putative source habitat. Of the 613 carp
(ranging in size from 151 to 894 mm total length;
mean = 328 mm TL) captured and implanted with
PIT tags in this pond, 80 carp (13%; TL: 183–723 mm;
mean: 350 mm) were recaptured in either Markham
Pond or Upper Kohlman Basin. Of those recaptured,
25 carp (TL: 304–628 mm; mean: 360 mm) had
emigrated from Markham Pond and were recaptured
in Upper Kohlman Basin, suggesting an emigration
rate of 25/80 or 31% of surviving individuals.
Confirming source–sink structure
across the watershed using genetics
Genetic variation and structure
Genetic variation at all 12 microsatellite loci from carp
(n = 1041) collected throughout the Phalen
Source–sink dynamics explain the distribution and persistence of an invasive population
123
Watershed was substantial and met assumptions for
STRUCTURE analysis of population structure and
ancestry assignment (details reported in Online
Resource 3). Bayesian clustering analysis in STRUC-
TURE revealed two genetically distinct strains of carp
within the watershed as indicated by values of -log
P(X/K) plateauing at K = 2 and strong support for
K = 2 from the rate of change of the likelihood
function (i.e., Evanno method; Fig. 2). We then used
NEWHYBRIDS probabilities to assign individuals to
either pure strain (hereafter referred to as ‘‘Strain A’’
and ‘‘Strain B’’), or hybrid crosses between strains and
compared these assignments among samples.
Distribution of carp genetic strains across space
and time
The genetic composition of the carp subpopulations in
putative source habitats (shallow ponds) and putative
sink habitats (lakes) showed different patterns. Of the
523 carp sampled in the main lakes (all lakes
combined), both genetic strains and their hybrids were
well-represented (Strain A, 19%; Strain B, 59%;
hybrid, 22%), whereas the Kohlman Creek and
Gervais Creek ponds each contained predominantly
one strain or hybrids (Fig. 3). Specifically, of the 209
carp sampled from ponds in the Kohlman Creek
subwatershed (Casey, Markham, and Upper Kohlman
Basin), the majority (81%) were Strain A and the
remaining individuals were classified as hybrid. No
individual captured in the Kohlman Creek subwater-
shed was classified as Strain B. Conversely, the ponds
in the Gervais Creek subwatershed (Interstate and
Gervais Mill) contained a majority of hybrids (64%)
and included the only pure Strain B carp (12%)
sampled in a putative source habitat patch.
The genetic assignment results of known-age
individuals in a random sample of 127 carp from the
main lakes revealed that the genetic composition of
the carp in the main lakes changed approximately
three decades prior to sampling. Ages of these carp
ranged from 3 to 64 years (median = 35 year,
mean = 31 year, Fig. 4), but multiple genetic strains
Table 2 Catch rates (# per net) of young-of-year common carp (\ 150 mm TL) sampled during standardized annual August trap-net
surveys from 2009 to 2013 in the Phalen Watershed
Location Site Habitat 2009 2010 2011 2012 2013
Kohlman Creek subwatershed Casey Pond 6.2 3.8 2.0 8.0 NS
Markham Pond 104.0 47.0 0.8 0.7 68.8
Upp. Kohlman Basin Pond 13.3 NS 0.6 1.7 0.7
Willow Pond 173.0 5.4 0.0 0.0 0.0
Gervais Creek subwatershed Interstate Pond NS NS NS NS 23.0
Owasso Basin Pond 3.1 NS 0.0 NS 0.0
Savage Pond 0.0 NS 0.0 0.0 0.0
Gervais Mill Pond 0.0 NS 0.0 0.0 1.0
Main chain of lakes Kohlman Lake 0.0 0.0 0.0 0.0 0.0
Gervais Lake 0.0 0.0 0.0 0.0 0.0
Keller Lake 0.0 0.0 0.0 0.0 0.0
Phalen Lake 0.0 0.0 0.0 0.0 0.0
NS denote sites that were not sampled. Catch rates from 2009 and 2010 are from Osborne (2012)
Fig. 2 Mean log-likelihood probability (Ln P (X/K); open
circles) and Evanno Delta K (squares) as a function of the
number of genetic clusters (K) averaged over five STRUCTURE
runs for each K ranging from 1 to 5
J. D. Dauphinais et al.
123
were not evident in the population prior to 1979.
Specifically, almost every individual older than
33 years old (n = 65 of 67) was classified as Strain
B whereas the majority of carp younger than 33
Fig. 3 The genetic
composition of common
carp sampled outside of the
spawning season in water
bodies of the Phalen
Watershed: a shallow ponds
of the Kohlman Creek
subwatershed (n = 209),
b shallow ponds of the
Gervais Creek subwatershed
(n = 70), c the main lakes
combined (n = 523), c1Kohlman Lake (n = 94), c2Gervais Lake (n = 347), c3Keller Lake (n = 52), and
c4 Phalen Lake (n = 30)
Fig. 4 The age structure
and genetic composition of a
randomly selected subset of
common carp (n = 127)
from lakes Kohlman,
Gervais, Keller, and Phalen
of the Phalen Watershed.
The genetic composition is
broken down by year class
Source–sink dynamics explain the distribution and persistence of an invasive population
123
(n = 60) were classified as Strain A (57%) along with
some Strain B (22%) and hybrid (21%) individuals
(Fig. 4). Two carp older than 33 years were classified
as hybrids but had 0.83 probability of assignment to
Strain B, suggesting possible classification error.
Because the Phalen Watershed only contained one
genetic strain (Strain B) of carp prior to 1979 (33 years
before 2012), we were able to infer the dispersal and
colonization of the younger Strain A individuals from
the Kohlman Creek subwatershed ponds to the main
lakes against the existing background of Strain B
ancestry. Notably, as the distance from the Kohlman
Creek subwatershed ponds increased, the proportion
of Strain A individuals decreased from 0.42 in Lake
Kohlman, to 0.16 in Lake Gervais, to 0.06 in Lake
Keller, and finally to 0.03 in Lake Phalen (Fig. 3c1–
c4).
Adult carp were observed spawning in all major
lakes and several ponds. The genetic composition of
reproductively mature and active carp captured in the
main lakes (putative sink habitats) during the spawn-
ing season was relatively similar to that of the resident
carp captured in the main lakes outside of the
spawning season (Strain A: B: Hybrid = 19%: 59%:
22% vs. 32%: 33%: 35%; Fig. 5). In contrast, the
reproductively mature carp that were captured migrat-
ing in Kohlman and Gervais Creeks attempting to
access the shallow ponds from the main lakes during
the spawning season, had substantially different strain
assignments than the resident carp captured in the
main lakes outside of the spawning season. Remark-
ably, the genetic composition of these carp closely
resembled those of the resident subpopulations within
each respective subwatershed into which they were
attempting to migrate (Fig. 5). Specifically, carp
caught during their spawning migration in Kohlman
Creek were mostly Strain A (79%) as were the resident
carp from the Kohlman Creek ponds (81%). Con-
versely, the carp caught during their spawning migra-
tion in Gervais Creek had a majority of hybrid
individuals (62%) as did the resident carp from these
ponds (64%; Fig. 5). All migrating adults sampled had
expressible gametes suggesting they were hours to
days from spawning.
Discussion
This study provides new empirical evidence that the
common carp, an important invasive fish, exhibits
source–sink population structure in a critical portion
of its invasive range, the headwaters of the Upper
Mississippi River Basin. We demonstrate both habitat-
specific recruitment rates across a heterogeneous
system of lakes and ponds and dispersal of carp from
source habitats to sinks using tagging and genetic data.
We conclude that differences in habitat quality,
specifically pertaining to carp recruitment success in
shallow lakes that experience hypoxia, create a
source–sink dynamic in which shallow, predator-free
ponds serve as productive sources and lakes serve as
demographic sinks. These findings support and expand
upon existing work demonstrating habitat-specific
recruitment rates in carp in North America (Bajer
and Sorensen 2010; Bajer et al. 2012; Silbernagel and
Sorensen 2013) and Australia (Driver et al. 2005;
Stuart and Jones 2006; Crook et al. 2013) and suggest a
new framework for understanding carp population
dynamics. This additional information enhances our
understanding of carp invasiveness in fragmented,
heterogeneous systems that typify both the regions
where carp evolved and where they now thrive, while
calling for a reexamination of conventional control
strategies that rely heavily on adult removal and have
largely failed (Weber and Brown 2009).
Our conclusion that carp in the Phalen Watershed
exhibit source–sink dynamics is based on 5 years of
data on adults and young across the entire system of
interconnected lakes and ponds. The distribution of
YOY carp, recoveries of tagged individuals, and
genetic data all indicate that shallow pond habitat
patches serve as sources, supplying carp to lake
habitats which would otherwise be demographic sinks.
Annual surveys for juvenile carp in every lake and
pond revealed that despite observations of spawning in
every basin, YOY carp were only present in select
shallow ponds, with no evidence that lakes produce
carp of their own. Without successful recruitment, the
lakes must be demographic sinks in the absence of
immigration. Our tagging study confirmed that shal-
low ponds serve as sources by documenting the
emigration of 31% of recaptured carp originally
tagged in Markham Pond. Given the estimated pop-
ulation size of over 2000 carp in Markham Pond at the
time of this study (Online Resource 1), this rate of
J. D. Dauphinais et al.
123
emigration from Markham Pond alone would be
enough to sustain a sizeable carp population in
connected lakes, especially given the longevity of
carp in this system (up to 64 years).
The spatial and temporal patterns of genetically
distinct carp across the Phalen Watershed also
strongly support the hypothesis that shallow pond
habitats function as sources from which carp recruits
disperse. In particular, because there was no evidence
of YOY carp in any of the main lakes and there were
genetically distinct subpopulations of carp in each
subwatershed, we were able to infer the natal sources
of carp sampled in the main lakes based on their
genetic assignments. It follows that Strain A individ-
uals originated from the nursery ponds in the Kohlman
Creek subwatershed and Strain B individuals
(b) Non-reproductive (a) Non-reproductive
Reproductive
(c) Non-reproductive
Reproductive Reproductive
Strain AHybridStrain B Temporary Fish barrier
N
Fig. 5 The genetic
composition of groups of
sexually-mature common
carp sampled during the
spawning season (May–
June; ‘‘reproductive’’) and
outside of the spawning
season (‘‘non-
reproductive’’) in: a the
Kohlman Creek
subwatershed, b the Gervais
Creek subwatershed, and
c the main lakes. The
spawning-season samples
from the Kohlman and
Gervais Creek
subwatersheds were
comprised of carp captured
during spawning migrations
from the main lakes towards
respective shallow pond
habitats. Arrows show
capture locations at
temporary fish barriers
installed across the streams.
The spawning-season
samples from the main lakes
were from carp that were
actively spawning (releasing
gametes) in littoral areas
Source–sink dynamics explain the distribution and persistence of an invasive population
123
originated from ponds in the Gervais Creek subwa-
tershed. Although hybrids were sampled in both
subwatersheds, the proportion of individuals classified
as hybrids in the Kohlman Creek subwatershed was
relatively low (19%) whereas hybrids made up the
majority of the Gervais Creek subwatershed samples
(64%). It is therefore reasonable to assume that many
of the hybrid individuals sampled in the main lakes
also originated from the Gervais Creek subwatershed.
The decreasing proportion of Strain A individuals in
each of the main lakes as distance from the Kohlman
Creek subwatershed increased provides further evi-
dence in support of carp dispersing from the shallow
ponds of Kohlman Creek and colonizing lake habitats
over time. Finally, the persistence of genetically
distinct strains of carp in the main lakes provides
further evidence that the lakes rely on inputs from
multiple sources instead of in-lake recruitment. Based
on the relatively high proportions of both strains of
carp observed actively spawning in the main lakes (32
and 33% pure Strain A or B, respectively), the lakes
would soon be dominated by hybrids if in-lake
recruitment were in fact successful (e.g. 87.5% of
offspring are expected to be hybrids if two strains at
equal proportions mate randomly for two genera-
tions). Because NEWHYBRIDS only considers first-
and second-generation hybrids, assignment error
would be expected if advanced-generation back-
crosses were present; however, based on the old age
of many individuals and relatively short time since the
strains have been mixed, there should have been few
advanced-generation hybrids in the population.
The unexpected finding of strongly differentiated
genetic strains of carp at a subwatershed scale likely
can be explained by changes to the system’s hydrology
and connectivity, and repeated introductions of this
species. Notably, Markham Pond was constructed in
the 1970s as a storm water retention basin and likely
enhanced connectivity between the ponds in the
Kohlman Creek subwatershed and the main lakes.
This is consistent with the age of the oldest Strain A
carp (age 33 in 2012) detected in the main lakes.
Several lines of evidence suggest Strain A derived
from a separate stocking of a genetically distinct
source into the Kohlman Creek subwatershed rather
than from bottlenecking and divergence from Strain B.
First, the program STRUCTURE estimated that Strain
A had 18 relatively common alleles that were not
likely in Strain B (allele frequency range 0.05–0.32 in
Strain A and 0–0.007 in Strain B). A bottlenecked
population should have a subset of the alleles found in
the source population. Second, Kohlman Creek pond
samples, which were predominantly Strain A, did not
have low diversity (Online Resource 3) as would be
expected following a bottleneck. Finally, strain A is
distributed across several age classes (Fig. 4) and not
the result of an isolated spawning event involving a
small number of families. The declining contribution
of Strain B over time may be explained by the
construction of the interstate system (I-35E) in the
1970s that reduced connectivity between the main
lakes and the ponds of the Gervais Creek
subwatershed.
Our analysis of the genetic composition of groups
of reproductively mature carp captured spawning or
making spawning migrations in different areas of the
watershed supports our hypothesis that only source
habitats contribute to overall metapopulation growth.
Additionally, this analysis revealed an unexpected
finding, the discovery of strain-specific migratory
behavior. The striking resemblance between the
genetic compositions of spawning groups migrating
from the main lakes up Kohlman and Gervais Creeks
to those of the resident subpopulations in each
respective subwatershed strongly suggests that carp
exhibit reproductive site fidelity. Although intra-
annual spawning site fidelity by carp has been
previously documented (Bonneau and Scarnecchia
2002) and homing behavior has been suggested by
Chizinski et al. (2016), this is the first evidence of
interannual reproductive homing, likely to natal sites.
The genetic differentiation that has persisted in the
Phalen Watershed over several decades would have
required ongoing reproductive isolation strong enough
to prevent genetic homogenization over time (Epi-
fanio and Philipp 2000). Our finding of\ 4% Strain B
individuals migrating up Kohlman Creek during the
spawning season is comparable to straying rates
reported for salmonids well-known for natal homing
behavior (Quinn 1993). Homing tendencies and partial
migrations of carp could be exploited for control by
trapping migrants in select corridors or by strategically
blocking access to high-quality nursery habitats
(Chizinski et al. 2016). Source–sink structured popu-
lations such as in the Phalen Watershed would be
especially vulnerable to exploitation because the
persistence of the entire metapopulation relies on the
contribution of specific source habitats.
J. D. Dauphinais et al.
123
Our findings complement recent research seeking
to explain carp invasiveness and inform effective
control strategies. Previous studies show that the
invasiveness of carp can often be attributed to
recruitment hotspots that serve as productive nurseries
across large spatial scales (e.g., Bajer and Sorensen
2010; Stuart and Jones 2006; Crook et al. 2013).
Related work provides evidence that carp recruitment
can be controlled by egg and larval predators in
portions of their invasive range, but that optimal
spawning habitats that lack predators often exist as
part of the landscape mosaic (Bajer et al. 2012, 2015a;
Silbernagel and Sorensen 2013). These studies also
speculate that such localized predator-free habitats are
the primary source of carp to connected waters, but did
not provide any direct evidence of dispersal as we
have. Our findings provide both direct tagging and
indirect genetic evidence of carp dispersal between
source and sink habitats, emphasizing the importance
of localized nursery habitats to population persistence
at the landscape scale. Our results indicate that
conventional control efforts such as mass harvesting
of adult carp in lake habitats are futile unless the
source habitats are first addressed. This conclusion is
consistent with a recent study by Weber et al. (2016)
that reported stable carp abundance despite harvesting
carp from three interconnected lakes over 5 years with
annual exploitation rates as high as 43%. Carp control
might thus be best accomplished by identifying critical
source habitats, suppressing recruitment, and disrupt-
ing dispersal between sources and sinks, before culling
adults from sink habitats. There are several manage-
ment approaches that could achieve these objectives
while minimizing impacts to non-target species. For
example, species-specific behaviors such as the timing
of migratory movements (Chizinski et al. 2016),
jumping and pushing abilities (Stuart et al. 2006;
Conallin et al. 2016), and sensitivity to sound (Zielin-
ski and Sorensen 2015) have been exploited to
selectively trap or deter migrating carp. Additionally,
recruitment suppression may be possible via well-
timed water-level manipulation (Yamamoto et al.
2006) or strategic spawning sabotage (Taylor et al.
2012).
Although source–sink dynamics may explain the
invasiveness of common carp in many complex
heterogeneous systems, this concept is not universally
applicable. For instance, the source–sink framework
would not apply to carp populations that lack
metapopulation structure or occur in homogenous
habitats such as lakes in the western plains of the
Midwest where carp recruitment dynamics seem to be
driven by other factors including high YOY survival
and lake productivity (Weber and Brown 2013; Bajer
et al. 2015a). Winter hypoxia and patchily distributed
predators is only one of many possible mechanisms
that may result in source–sink dynamics. In riverine
systems of Australia, for example, alternative mech-
anisms such as flooding or flow diversion may lead to
habitat-specific carp recruitment and mortality rates
(Driver et al. 2005; Macdonald and Crook 2014). It is
also possible for source–sink dynamics to vary in
intensity over time (Johnson 2004), and in extreme
cases, for source–sink inversion to occur where former
source populations are extirpated and recolonized by
extant subpopulations in sink patches (Dias 1996;
Boughton 1999). This phenomenon may occur when
source habitat patches are more vulnerable to envi-
ronmental extremes or other perturbations relative to
more stable sink habitats (Frouz and Kindlmann
2001). The disappearance of carp from Willow Pond
during our study period coupled with the large
variation in observed recruitment rates over time and
space exemplifies the complexity associated with
choosing a proper spatial and temporal scale at which
to evaluate source–sink metapopulation processes.
Understanding the factors that influence population
structure and persistence at relevant spatial and
temporal scales is paramount for effective manage-
ment. Our study emphasizes the importance of habitat
heterogeneity and connectivity in regulating fish
metapopulation dynamics and draws attention to the
utility of the source–sink framework for invasive
species management. This framework has been
applied successfully to control common carp in the
Phalen Watershed (W. Bartodziej, Ramsey-Washington
Metro Watershed District, Little Canada, MN USA,
unpublished data). Source populations were elimi-
nated from Casey and Markham Ponds via water
drawdowns in 2013 and 2014, respectively. These
ponds were then aerated and stocked with native
bluegill sunfish to provide biocontrol in the event of
re-colonization by carp. To date, annual trap-net
surveys have not found any YOY carp since the
drawdowns. With most of the ongoing recruitment
under control, the carp population in the main lakes
was reduced via trapping of spawning migrants in
Kohlman Creek and commercial harvest. Because the
Source–sink dynamics explain the distribution and persistence of an invasive population
123
main lakes function as demographic sinks in the
absence of immigration, culling adults from these
habitats should provide long-term control at the
metapopulation level barring an influx of new recruits.
Future research is needed to identify sources, sinks,
and dispersal pathways for carp in other locations
across the globe and for additional invasive species.
The source–sink framework has been indispensable
for conservation planning over the last few decades
(Loreau et al. 2013; Furrer and Pasinelli 2015) and its
tenets and tools should not be overlooked when
attempting to understand and control invasive
populations.
Acknowledgements This work was funded by the Ramsey-
Washington Metro Watershed District (RWMWD). We thank
Nathan Berg, Justin Howard, Jacob Osborne, Mary Headrick,
Brett Miller, Seth Miller, and Danielle Grunzke for assistance
with fieldwork and laboratory analyses. We would also like to
thank RWMWD staff, specifically Bill Bartodziej and Simba
Blood, for project coordination and support. We thank Jessica
Eichmiller and three anonymous reviewers for their helpful
comments.
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