Download Reiskind, M.H. and M.L. Wilson. 2008. Interspecific

POPULATION AND COMMUNITY ECOLOGY
Interspecific Competition Between Larval Culex restuans Theobald
and Culex pipiens L.(Diptera: Culicidae) in Michigan
MICHAEL H. REISKIND1,2
AND
MARK L. WILSON1,3
J. Med. Entomol. 45(1): 20Ð27 (2008)
ABSTRACT Many invasive species succeed in becoming established in new locations because of
their competitive superiority to native species. This has been shown in several examples involving
mosquitoes. In this study, we examined the interspeciÞc competition between mosquito larvae of a
well-established, non-native species, Culex pipiens, and those of its ecologically similar, native congener Culex restuans. Small but signiÞcant differences in survival, growth, and development rates were
found in Cx. restuans as a response to varying proportions of Cx. pipiens, suggesting that Cx. restuans
is a slightly superior competitor. However, the overall differences between the species were small, and
they may be nearly ecological equivalents as larvae. Nevertheless, the observed seasonal pattern of
feeding and oviposition activity suggests some phenological avoidance of competition, thus demanding
further study of the interaction of these two species.
KEY WORDS phenology, invasion biology, West Nile virus, ecological equivalence, larval competition
Invasive species may successfully establish in novel
locations because of a superior competitive ability
relative to ecologically similar native species, allowing
such invaders to competitively displace the natives
(Connell 1980, Simberloff and Boecklen 1991, Mack et
al. 2000, Tilman 2004). Other reasons for an invasive
speciesÕ success may be the exploitation of unoccupied
niches or newly created habitats (Mack et al. 2000).
Many studies have examined currently or very recently invading mosquito species, but there is considerably less work on known invasive species that are
already well established. In this study, we examined
the potential for competition at the larval stage between a North American native species of mosquito,
Culex restuans Theobald, and a naturalized European
species, Culex pipiens pipiens L. (Ross 1964). Because
both of these species are involved in West Nile virus
transmission, understanding their ecology is important
in characterizing how they may affect West Nile epidemiology (Nasci et al. 2001). Furthermore, studying
this past invasion may provide insights into the ongoing introductions of several other mosquito species in
North America.
The cosmopolitan species Cx. pipiens probably arrived in North America from Europe around the time
of the early European settlers, ⬇400 yr ago (Fonseca
et al. 2004). On arrival to the new world, Cx. pipiens
encountered a native mosquito fauna, including Cx.
restuans, a species of similar ecology. Cx. pipiens
1 Department of Ecology and Evolutionary Biology, The University
of Michigan, Ann Arbor, MI 48104.
2 Corresponding author: Florida Medical Entomology Laboratory,
200 9th Street SE, Vero Beach, FL 32962 (e-mail: mhayr@uß.edu).
3 Department of Epidemiology, School of Public Health, The University of Michigan, Ann Arbor, MI 48104.
spread across the continent with European colonization, generating the current pattern of widespread
distribution of this mosquito throughout most of North
America and producing considerable overlap with Cx.
restuans (Covell and Resh 1971, Darsie and Ward 1981,
Jackson et al. 2005). Studies on the ecology of these
mosquitoes suggest that they have some degree of
seasonal separation, with adult C. restuans generally
abundant in the early summer and Cx. pipiens more
abundant in the late summer and early fall (Madder et
al. 1980, Lampman and Novak 1996, Lee and Rowley
2000, Jackson and Paulson 2006). However, they usually overlap in late summer or early fall, depending on
the particular location.
Larval Cx. restuans and Cx. pipiens appear to be
ecologically similar, as both Þlter-feed in open water
and have similar mouthpart morphology. However,
little is known about Cx. restuans feeding, which may
differ from that of Cx. pipiens, because Cx. pipiens
primarily exploit free-swimming bacteria and protists
(Thiery et al. 1991, Clements 1993). Previous research
has shown that water volume and concentration of
nutrients are important to growth and survival of Cx.
restuans (Reiskind et al. 2004), and density-dependent
reductions in growth and survival at the larval stage
have been documented for Cx. quinquefasciatus, a sibling species to Cx. pipiens (Rajgopalan et al. 1976,
Agnew et al. 2000, Mpho et al. 2000).
InterspeciÞc competition is well known in containerbreeding mosquitoes, even to the point of competitive displacement of resident species by invasives.
One particularly well-studied system is the invasive
Aedes albopictus and its interactions with established
North American mosquito species. Several studies
have investigated interactions between Ae. albopictus
0022-2585/08/0020Ð0027$04.00/0 䉷 2008 Entomological Society of America
January 2008
REISKIND AND WILSON: COMPETITION BETWEEN Culex SPP.
and Aedes aegypti, generally concluding that Ae. albopictus larvae are superior competitors under realistic conditions, allowing them to displace Ae. aegypti
from much of its previous range (OÕMeara et al. 1995,
Juliano 1998, Daugherty et al. 2000, Juliano et al. 2002).
Likewise, studies have examined competition of Ae.
albopictus with Aedes triseriatus and Cx. pipiens (Ho et
al. 1989, Livdahl and Willey 1991, Sota 1993, Edgerly
et al. 1999, Carrieri et al. 2003, Constanzo et al. 2005b).
Under realistic, Þeld-like conditions, the invasive Ae.
albopictus was the superior competitor in these studies
as well. However, several studies and Þeld observations suggest the competitive outcome does not necessarily lead to competitive displacement and may
result in coexistence (Black et al. 1989, Livdahl and
Willey 1991, OÕMeara et al. 1995, Edgerly et al. 1999).
In California, where Cx. quinquefasciatus is invading
new areas, it was observed to be the superior competitor to Cx. tarsalis, a native species, and replaced Cx.
tarsalis in one generation under laboratory conditions
(Smith et al. 1995). Another study compared Cx. quinquefasciatus and Cx. pipiens molestus larval competition in Iraq, concluding that Cx. quinquefasciatus was
the superior competitor but without making reference
to differences in ecology between these species
(Mohsen and Al-Saady 1995). However, there have
been no studies examining the nature of competition
between Cx. restuans and Cx. pipiens larvae, despite
their common co-occurrence in North America and
importance in West Nile virus transmission (Nasci et
al. 2001, Spielman et al. 2004).
Understanding the nature of interspeciÞc competition between these two species is important for a
number of reasons. First, if they are strong competitors, this may help explain the differences in seasonal
activity. The different seasonal activity patterns of
these two species, in turn, may inßuence the epidemiology of bird-derived vector-borne viral encephalitides. For example, both of these species have been
implicated as important vectors of West Nile virus in
the northern United States, with Cx. restuans being the
likely vector in bird populations, and Cx. pipiens involved in both bird transmission and as a bridge vector
between birds and mammals (Apperson et al. 2002).
The rise in human cases during late fall is temporally
consistent with greater abundance and activity of Cx.
pipiens during this period (Spielman et al. 2004, Lampman et al. 2006). Second, although these species often
co-occur, there may be spatial differences in their
abundance, which could be explained by interspeciÞc
competition between larvae (Yee and Yee 2007). Finally, studying historical biological invasions can provide insight into the endpoint of ongoing invasions,
such as that by Ae. japonicus in the eastern United
States and Ae. albopictus throughout the Midwest
(Alto and Juliano 2001). Recent theoretical advances
in our understanding of evolution and competitive
displacement propose that, given sufÞcient time, competitors may evolve toward increasing “equivalence,”
although explicit predictions remain difÞcult to make
(Leibold and McPeek 2006).
21
Considering the similarity in larval ecology, the establishment of Cx. pipiens throughout North America
suggests it may compete (or may have competed) with
Cx. restuans. However, Cx. pipiens may have occupied
a new niche, or both species may have evolved to a
point of little niche overlap, sensu Leibold and McPeek
(2006). Regardless of the historical circumstances, the
question of interspeciÞc competition between these
species remains unexplored and interesting. If the
hypothesis of superior larval competition is correct, in
situations in which Cx. restuans larvae are relatively
more abundant than Cx. pipiens conspeciÞcs, Cx. pipiens should have higher emergence rates, grow larger,
and emerge sooner (intraspeciÞc competition ⬎ interspeciÞc competition for Cx. pipiens, with the opposite for Cx. restuans). Conversely, when Cx. pipiens
larvae encounter more conspeciÞcs, they should have
lower emergence rates, grow less, and emerge later.
Materials and Methods
Larval Source
Culex spp. egg rafts were collected from three sites
in Ann Arbor, MI, Ruthven Park, Hannah Park, and
Dolph Park, from hay-baited ovitraps described elsewhere (Reiskind and Wilson 2004). Egg rafts were
transported to the laboratory in 18-well tissue culture
plates (Fisher, Pittsburgh, PA), with a single egg raft
in each well. On hatching, Þrst-instar larvae were
identiÞed to species and separated using the presence
of a clear scale anterior to the sclerotorized eggbreaker for Cx. restuans and the lack of this character
for Cx. pipiens. Previous observations have shown that
this is a good character for separating these two species, and it was conÞrmed using a polymerase chain
reaction (PCR)-based molecular identiÞcation technique (Crabtree et al. 1995).
Experimental Design
The overall design is a replacement series, in
which the density of the competitors is kept constant while the ratio of one to the other changes.
We conducted this at two volumes of media, previously shown to be important in larval development (Reiskind et al. 2004).
Experiment 1: High Volume. Individual egg rafts
(n ⫽ 41) collected on 3 August 2004 were held at 22⬚C,
in the water they were collected from until they
hatched on 4 August 2004, and identiÞed as either Cx.
pipiens (5/41) or Cx. restuans (36/41). On identiÞcation on 4 August, larvae were pipeted into a container
of conspeciÞcs with 250 ml distilled water and 4 g of
ground TetraMin Fish Food (Tetra, Melle, Germany).
The following day, 20 larvae were placed in each
individual 500-ml plastic, food grade container with
200 ml of well water infused over the previous 24 h
with organic, pesticide-free grass hay at a concentration of 10 g/liter. This relatively low concentration was
used because previous experiments suggested that
competition would be more apparent (Reiskind et al.
22
JOURNAL OF MEDICAL ENTOMOLOGY
2004) For all experiments, the following combinations
of Culex larvae were used: 20 restuans; 15:5 restuans:
pipiens; 10:10 restuans:pipiens; 5:15 restuans:pipiens;
and 20 pipiens. Each of these combinations was replicated 10 times. All incubator conditions for larval
development were identical for all experiments (14
L:10 D; 22:16⬚C). Time to pupation and eclosion were
recorded for 20 d (5Ð24 August 2004). All adults were
caught and killed by freezing. Adults were dried at
48⬚C for 48 h and weighed using a Cahn electro-micro
balance (Cahn Instrument Co., Paramount, CA). Females were identiÞed morphologically to species using
the presence of two obvious gold spots on the scutum
as the principle character for Cx. restuans and a uniform, light-brown to golden scutum for Cx. pipiens
(Darsie and Ward 1981). Males were identiÞed by
dissection of genitalia (Means 1987).
Experiment 2: Low Volume. A low nutrient volume
experiment using 100-ml water volumes instead of 200 ml
(with the same size and shape containers as previously
used) was conducted for 20 d from 18 August to 7 September 2004. Because the containers were slightly ßuted,
there were small differences in surface area between the
low and high volume treatments (at 100 ml, SA ⫽ 289.4
cm2; at 200 ml, SA ⫽ 333.1 cm2). Larvae were collected
on 16 August 2004 and treated in the same manner as in
the high-nutrient experiment. Of 56 rafts collected, 16
were identiÞed as Cx. pipiens and 40 as Cx. restuans. Time
to pupation and eclosion, percent emergence, and adult
weights were measured as above.
Statistical Analysis
To analyze the overall effects of volume and competition on survival, we followed the recommendations of Goldberg and Scheiner (2001) and used a
two-way analysis of variance (ANOVA) for each species separately, with sexes combined. Because of poor
survivorship at low volume, similar analyses of weight
and days to emergence were not possible. Outcomes
assessed for the high-volume experiments were days
to emergence, survivorship (percent emergence, arcsine and square-root transformed to approximate a
normal distribution), and dry weight (mg). Both
males and females of both species from the highvolume experiment were analyzed, using multivariate
ANOVA (MANOVA) on all outcomes (Scheiner
2001). The canonical function loadings from the
MANOVAs describe the importance of each outcome
on the overall effect of competition. All statistical
analyses were conducted using SAS (SAS, Cary, NC).
Results of one-way ANOVAs, after a signiÞcant
MANOVA, from the high-volume experiment are presented as increasing ratios of conspeciÞcs to hetereospeciÞcs, such that data at each ratio come from
different containers, except in the 10 conspeciÞcs:10
hetereospeciÞcs treatment. Statistical comparisons
are separate for each species between different levels
of interspeciÞc competition.
Vol. 45, no. 1
Table 1. Two-way ANOVA comparing volume and competition effects
Source
Culex restuans
Volume
Competition
Volume ⫻ competition
Error
Culex pipiens
Volume
Competition
Volume ⫻ competition
Error
df
F
P
1
3
3
73
156.89
3.16
1.44
⬍0.0001
0.0299
0.2386
1
3
3
73
60.85
2.39
1.89
⬍0.0001
0.0754
0.1392
Results
Effects of Nutrient Volume and Competitive
Environment
The volume of nutrients signiÞcantly affected survivorship in both species with both sexes combined (Table
1). Survivorship in Cx. restuans was signiÞcantly affected
by proportion of Cx. pipiens across volumes (competition: Fdf ⫽ 3 ⫽ 3.16, P ⫽ 0.0299), whereas survivorship in
Cx. pipiens was not signiÞcantly affected by Cx. restuans
(competition: Fdf ⫽ 3 ⫽ 2.39, P ⫽ 0.0754). There was no
signiÞcant interaction term between volume and competitive treatment for either species.
Effects of Interspecific Competition on Cx. restuans
at High Volume
All three outcomes (days to emergence, percent
emerged, and adult weight) were signiÞcantly affected for Cx. restuans females depending on degree of
interspeciÞc competition (MANOVA, PillaiÕs trace ⫽
0.745, F9,99 ⫽ 3.63, P ⫽ 0.0006). In the Þrst canonical
coefÞcient, which explained 60.4% of the variation,
weight was over twice as important as emergence rate,
which was more important than time to emergence
(Table 2). For the second canonical coefÞcient, explaining 36.4% of the variation, all three factors loaded
Table 2. Standardized canonical coefficients on the three canonical functions for days to emerge, percent emergence (on arcsin, square root-transformed data), and adult weight, from the
MANOVA for Cx. restuans and Cx. pipiens females
Outcome
Cx. restuans
Days to emerge
Emergence rate
Weight
Percent of variation
explained
F-value
P value
Cx. pipiens
Days to emerge
Emergence rate
Weight
Percent of variation
explained
F-value
P value
Canonical
1
Canonical
2
Canonical
3
⫺0.185
0.422
1.059
60.41
0.813
⫺0.889
0.877
36.40
1.019
0.516
0.542
0.032
3.86
0.0005
⫺0.204
1.247
⫺0.422
95.91
2.87
0.0071
3.46
0.0135
0.977
⫺0.032
0.098
0.04
0.34
0.8472
1.22
0.27
⫺0.05
0.627
0.985
0.00
0
0.9918
January 2008
A
REISKIND AND WILSON: COMPETITION BETWEEN Culex SPP.
0.5
B
0.45
0.4
Weight (mg)
23
0.35
AB
AB
15:05
10:10
A
0.3
0.25
0.2
0.15
0.1
0.05
0
20:00
B
0.35
Emerged (%)
05:15
0.4
A
A
0.3
b
Cx. restuans
AB
0.25
B
0.2
b
Cx. pipiens
0.15
0.1
a
a
0.05
0
20:00
Days to Emergence
C
15:05
10:10
05:15
16
14
12
10
8
6
4
2
0
20:00
15:05
10:10
05:15
Ratio of Conspecifics : Hetereospecifics
Fig. 1. Outcomes of high nutrient volume and interspeciÞc competition between Cx. restuans (gray bars) and Cx. pipiens
(hatched bars) on female mosquitoes. (A) Growth (as measured by dry weight of adult). (B) Percent emerged (of all possible
mosquitoes, both sexes). (C) Days to emergence from hatching. Letters denote homogenous groups by post hoc tests after
a signiÞcant one-way ANOVA using BonferroniÕs correction for multiple comparisons within each species separately (capital
letters for Cx. restuans, lowercase letters for Cx. pipiens).
almost equally. Overall, the canonical analysis suggests
weight and percent emergence were the most important factors, and the individual ANOVAs of each outcome agreed with this assessment (Fig. 1, A and B, gray
bars). Days to emergence was also important but relatively less so than the other two factors (Table 2; Fig.
1C, gray bars). There were no signiÞcant effects of
level of interspeciÞc competition on outcomes for
male Cx. restuans (MANOVA, PillaiÕs trace ⫽ 0.256,
F ⫽ 1.03, P ⫽ 0.4236). This is consistent with the
Þnding that individual ANOVAs for each outcome
were not signiÞcant (Fig. 2, AÐC, gray bars).
Effects of Interspecific Competition on Cx. pipiens
at High Volume
The overall effect of interspeciÞc competition on
all outcomes for Cx. pipiens females was signiÞcant
24
JOURNAL OF MEDICAL ENTOMOLOGY
A
Vol. 45, no. 1
0.45
0.4
Weight (mg)
0.35
0.3
0.25
0.2
0.15
0.1
0.05
0
20:00
B
15:05
10:10
05:15
0.5
0.45
Emerged (%)
0.4
0.35
0.3
0.25
0.2
Cx. restuans
0.15
Cx. pipiens
0.1
0.05
0
20:00
Days to Emergence
C
15:05
10:10
05:15
18
B
16
AB
14
12
AB
A
10
8
6
4
2
0
20:00
15:05
10:10
05:15
Ratio of Conspecifics : Hetereospecifics
Fig. 2. Outcomes of high nutrient volume and interspeciÞc competition between Cx. restuans (gray bars) and Cx. pipiens
(hatched bars) on male mosquitoes. (A) Growth (as measured by dry weight of adult). (B) Percent emerged. (C) Days to
emergence from hatching. Letters denote homogenous groups by post hoc tests after a signiÞcant one-way ANOVA using
BonferroniÕs correction for multiple comparisons within each species separately (capital letters for Cx. restuans, lowercase
letters for Cx. pipiens).
(MANOVA, PillaiÕs trace ⫽ 0.619, F9,78 ⫽ 2.25, P ⫽
0.026). Only the Þrst canonical coefÞcient explained
a signiÞcant amount of varation, with emergence
rate being a much larger contributor than the other
two outcomes (Table 2). Individual ANOVAs on
each outcome showed that only emergence rate was
signiÞcantly affected by level of interspeciÞc competition (one-way ANOVA, F3,26 ⫽ 9.32, P ⬍ 0.0002;
Fig. 1B, hatched bars). Overall effects of interspe-
ciÞc competition on male Cx. pipiens outcomes were
marginally nonsigniÞcant (MANOVA, PillaiÕs trace ⫽
0.457, F9,90 ⫽ 1.80, P ⫽ 0.0790). Individual ANOVAs on
each outcome showed a signiÞcant effect of interspeciÞc
competition on days to emergence (one-way ANOVA,
F3,30 ⫽ 4.20, P ⬍ 0.01; Fig. 2C, hatched bars) and a
marginally nonsigniÞcant effect on percent emerged
(arcsine, square root-transformed data, one-way
ANOVA, F3,30 ⫽ 2.63, P ⬍ 0.06; Fig. 2B, hatched bars).
January 2008
REISKIND AND WILSON: COMPETITION BETWEEN Culex SPP.
Discussion
Different ratios of conspeciÞcs to hetereospeciÞcs
signiÞcantly affected the outcome of competition between Cx. restuans and Cx. pipiens females. There was
no evidence that larval Cx. pipiens were superior competitors to Cx. restuans, which is contrary to our hypothesis. The only signiÞcant outcome for Cx. pipiens
females that varied with the ratio of conspeciÞcs to
hetereospeciÞcs was percent emerging, and in a manner that suggests stronger intraspeciÞc than interspeciÞc competition. At high volume, Cx. restuans females
showed more consistent results, again with evidence
that intraspeciÞc competition was stronger than interspeciÞc competition, particularly in the effects on
growth. Overall, these data suggest that Cx. restuans
may be a slightly better competitor, although the differences in larval competitive ability between the species were small. The situation in which intraspeciÞc
competition is stronger than interspeciÞc competition
for both species suggests some degree of niche separation, even in the controlled setting of these experiments, and may mean a stable coexistence between
the species (Vandermeer and Goldberg 2003).
There are several possible explanations for small
differences in competitive ability between two species
that seemingly share a similar niche. These two species
may be acting as ecological equivalents (Hubbell
2001), in which neither has a competitive superiority,
but they are still in stable coexistence because of
spatial or historical reasons. However, it has been
suggested that this is unlikely for invasive species,
because they may not be adapted to their new ecosystems (Leibold and McPeek 2006). In this case, Cx.
pipiens may have had sufÞcient time to adapt to its
North American environment and therefore become
increasingly equivalent to Cx. restuans. As suggested
by Leibhold and McPeek (2006), competitive exclusion is most easily observed early during invasions.
Indeed, in the Culicidae, competitive displacement
has been observed in the invasion of Aedes albopictus
in North America and its interactions with its naturalized congener Ae. aegypti (Lounibos 2002, Juliano
and Lounibos 2005).
Alternatively, these two species might have little
overlap under natural conditions, although there is
considerable evidence for sympatry (Darsie and Ward
1981, Jackson and Paulson 2006, Lampman et al. 2006).
Differences in the seasonal abundance of these two
species in much of their range are well documented,
and it is possible they do not encounter each other
sufÞciently often to differentiate through competitive
exclusion. However, larvae are often found together,
although they show slight differences in oviposition
preference (Covell and Resh 1971, Jackson et al. 2005,
Jackson and Paulson 2006). They may be subdividing
habitat in ways not easily observable, such as foraging
on different types of microorganisms or using different
foraging techniques (e.g., pure Þlter feeding versus
scraping surfaces). Behavior was not observed during
these experiments, but other researchers have found
25
variation among Culex species (Workman and Walton
2003).
Perhaps the conditions under which competition
was assessed were inadequate to detect species differences in competitive ability that might be observed
by studying the entire life cycle of both species (Constanzo et al. 2005a) or making observations under
more realistic conditions. Although incubator-based,
hay infusion containers are commonly used in oviposition studies (Reiter 1987, Reiskind and Wilson 2004),
this condition may not capture the intrinsic complexity of most natural habitats, such as diversity of microorganisms and nutrient quality, thus masking interspeciÞc interactions that occur under natural
conditions.
Although competition at the larval stage has been
shown to be important in determining species replacements and subsequent distributions in invasive culicids (Smith et al. 1995, Lounibos 2002), our study did
not document clear evidence for competitive superiority of the invasive Cx. pipiens. There was some evidence for competitive superiority of Cx. restuans (the
higher emergence rate at lower levels of intraspeciÞc
competition), but the differences between the species
were small. These two species show a profound seasonal separation where they co-occur, and the larval
superiority of Cx. restuans may have pushed Cx. pipiens
to breed late in the summer and into early fall.
Whether the “ghost of competition past” (Connell
1980) can explain the seasonal separation of these two
species remains to be tested.
Acknowledgments
We thank G. Newman for diligent assistance in this
project. The Natural Areas Preservation Unit (Ann Arbor
Parks Department) allowed us permission to undertake Þeld
studies on their properties. We also thank R. Barbehenn
(University of Michigan) for use of the electrobalance and B.
West (Center for Statistical Counseling and Research, University of Michigan). Furthermore, we thank B. W. Alto and
two anonymous reviewers for perceptive and helpful comments in preparing this manuscript. The University of Michigan Department of Ecology and Evolutionary Biology
(M.H.R.) and the Global Health Program (M.L.W.) provided
support for these studies.
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Received 4 May 2007; accepted 23 August 2007.