Lady Beetles in New York: Insidious Invasions, Erstwhile
Extirpations, and Recent Rediscoveries
John E. Losey, Leslie L. Allee, Erin Stephens, Rebecca R. Smyth, Peter Priolo, Leah Tyrrell, Scott Chaskey, and Leonard Stellwag
Northeastern Naturalist, Volume 21, Issue 2 (2014): 271–284
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2014 NORTHEASTERN NATURALIST 21(2):271–284
Lady Beetles in New York: Insidious Invasions, Erstwhile
Extirpations, and Recent Rediscoveries
John E. Losey1, Leslie L. Allee1,*, Erin Stephens1, Rebecca R. Smyth1,
Peter Priolo2, Leah Tyrrell1, Scott Chaskey3, and Leonard Stellwag1
Abstract - Over the past 40 years, the complex of coccinellid (lady beetle or ladybug)
species in New York has undergone substantial changes. Primarily, these changes have
involved the decline of native species and the increase and spread of adventive species.
Species declines have proceeded to the extent that several native species were feared to be
extirpated from New York. Here we report that two of these native species, Adalia bipunctata
(Two-spotted Lady Beetle) and Coccinella novemnotata (Nine-spotted Lady Beetle),
were rediscovered in New York, in 2009 and 2011, respectively, by volunteers and specialists
working for the Lost Ladybug Project. We found that the current coccinellid complex
in New York is significantly less diverse and has a significantly higher proportion of foreign
species compared to the complex in the past. We discuss the potential causes and implications
for these shifts and rediscoveries.
Introduction
Coccinellids (lady beetles or ladybugs) are important predators in both natural
and agricultural habitats. They provide the ecosystem service of controlling herbivorous
insects (Hodek et al. 2012). In agricultural habitats, coccinellids prey
on many economically important pests including aphids and other soft-bodied insects
(Metcalf et al. 1994). Coccinellids are common and economically important
predators in Zea mays L. (Corn) agroecosystems, preying upon pests of primary and
secondary importance, including aphids and Ostrinia nubilalis (Hübner) (European
Corn Borer) larvae and eggs (Gordon 1985). In natural areas, coccinellids suppress
outbreaks of a variety of herbivores and many species of aphids (Pack 1925).
Because coccinellids are vulnerable to limiting factors such as natural enemies,
introduced competitors, and other anthropogenic influences, they are recognized as
important bioindicators (Iperti 1999).
Numerous studies have examined the composition of the coccinellid complex,
and a smaller but no less important body of literature has related their density and
diversity to ecological function. Previous work has shown that coccinellid species
vary widely in the level of suppression they exert on various prey species (reviewed
in Hodek et al. 2012) and in their response to environmental changes (Bazzocchi et
al. 2004, Iperti 1999). These findings imply that long-term regional shifts in coccinellid
species composition may result in important changes in the functioning of
this complex and its response to environmental changes.
1Lost Ladybug Project, The Old Insectary, Department of Entomology, Cornell University,
Ithaca, NY 14853. 282 Chichester Avenue, Center Moriches, NY 11934. 3Quail Hill Farm,
Amagansett, NY 11930. *Corresponding author - LLA1@cornell.edu.
Manuscript Editor: Dan Pavuk
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Twenty-six of the more than 500 coccinellid species of North America north
of Mexico are exotic and were introduced for biological control (Gordon 1985,
Hodek et al. 2012). Three of the most successful and widely established introduced
coccinellids are Coccinella septempunctata (Seven-spotted Lady Beetle), Propylaea
quatuordecimpunctata (Fourteen-spotted or Checkerspot Lady Beetle), and
Harmonia axyridis (Multicolored Asian Lady Beetle), which were first established
in North America in 1973, 1972, and 1988, respectively (Gordon and Vandenberg
1991). Multicolored Asian Lady Beetle and Seven-spotted Lady Beetle, are active
and aggressive predators (Angalet et al. 1973, Cottrell and Yeargan 1998) that are
well adapted to disturbed habitats in a variety of climate conditions.
Over the last 30 years, these introduced coccinellid species increased rapidly
in both range and density, while several common native species of coccinellids
went through dramatic and as yet not well-explained population declines (Harmon
et al. 2007, Wheeler and Hoebeke 1995). Adventive coccinellids have been implicated
as factors contributing to the decline of native species (Obrycki et al. 2000,
Wheeler and Hoebeke 1995). Several studies have documented the propensity of
these introduced species to affect the ecology of native species, especially due to
intraguild predation (IGP) in the larval stage (Cottrell and Yeargan 1998, Elliot et al.
1996, Obrycki et al. 1998). In contrast, several other studies have shown relatively
uniform effects of IGP between native and introduced species (Gagnon et al. 2011,
Gardener et al. 2011). Most recently, a secondary mechanism has been proposed by
European researchers to explain the success of Multicolored Asian Lady Beetle in
Europe and the decline of Seven-spotted Lady Beetle, a species native to Europe,
as a result of IGP: Multicolored Asian Lady Beetle is immune to but carries lethal
microsporidia that are ingested by the susceptible Seven-Spotted Lady Beetle during
IGP (Vilcinskas et al. 2013). While the mechanisms of each species interaction
are not yet clear, Harmon et al. (2007) showed that introduced species were making
up an increasingly large component of many communities, and that many formerly
dominant coccinellids were no longer collected, including Coccinella novemnotata
(Nine-spotted Lady Beetle), Coccinella transversoguttata (Transverse Lady Beetle),
Adalia bipuncatata (Two-spotted Lady Beetle), and Hippodamia convergens
Guérin-Méneville (Convergent Lady Beetle). These changes have been a cause for
concern because most effective pest suppression comes from a diverse complex of
coccinellid species that includes native species (Snyder 2009).
Increased dominance of introduced species and decline of native species have
been especially pronounced in the northeastern US (Harmon et al. 2007, Wheeler
and Hoebeke 1995). The original range of the native species Nine-spotted Lady
Beetle and Two-spotted Lady Beetle included NY and the entire Northeast (Gordon
1985). In 2008, the Lost Ladybug Project (LLP), a citizen-science program
designed to recruit volunteers to gather data on the current status of coccinellids in
North America, was launched. As of June 2012, the LLP had over 17,000 identified
images of individual coccinellids, each of which was connected with collection
data. New York is particularly well represented in that database, with over 1400 observations.
In this paper, we combine the LLP data with data from Stephens (2002)
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to elucidate changes in the coccinellid complex in New York and similar changes
that have occurred throughout the Northeast US.
Field-Site Descriptions
Volunteers participating in the LLP surveyed Coccinellids across New York.
We targeted two areas for increased sampling effort following the rediscovery
of rare native species by volunteers at these sites. These two field sites are described
below.
The research survey area where Nine-Spotted Lady Beetle was found includes
the vegetable and flower plots of Quail Hill Farm, an organic farm in the Long
Island town of Amagansett, NY (40°97'36"N, 72°14'42"W). Long Island is in the
North Atlantic coastal ecoregion and is characterized by grasslands, shrublands,
vast pine barrens, coastal plain ponds, dunes, and extensive salt marshes. This
ecoregion differs from more southern coastal ecoregions by having coarser-grained
soils and Quercus (oak)-Pinus (pine) vegetation; it has less flat physiography than
the middle Atlantic coastal plain, but is more uniform than the northeastern coastal
zone. The main soil type, Bridgehampton silt loam, is well drained and occurs
on 0–2% slopes with silty glaciolacustrine or eolian parent material underlain by
contrasting glacial drift, derived mainly from gneiss, granite, and schist with some
sandstone, conglomerate, and shale. The typical profile is: 0–28 cm silt loam,
28–142 cm silt loam, and 142–203 cm stratified gravelly sand. Average elevation
is 9 m. Located in the USDA growing zone 7a (-17 °C to -15 °C annual minimum
temperature), this area has a mean annual precipitation of 114–127 cm, a mean annual
air temperature of 10–12 °C, and a frost-free period of 150–225 days with the
average first frost in mid-November and the average last frost i n mid-April.
The research area where surveyors found Two-spotted Lady Beetle is in the
residential area surrounding Buffalo State University in Buffalo, NY (42°88'64"N,
78°87'86"W). The Great Lakes ecoregion is glaciated with gently rolling hills and
irregular flat lake plains. It has a high level of biodiversity and unique habitats with
a climate influenced by the Great Lakes (NYS DEC n.d.). This region differs from
the northeastern highlands, northern Appalachian Plateau, and uplands ecoregions
because it generally has less surface irregularity and more agricultural activity
and population density. Land use in the Lake Erie plain watershed basin surrounding
Buffalo is dominated by agriculture associated with dairy operations but also
contains orchards, vineyards, and vegetable farms. Because Buffalo is close to
Lake Erie, it has an increased growing season, more winter cloudiness, and greater
snowfall than surrounding areas. The main soil type, Urban-Churchville complex,
has a parent material of clayey glaciolacustrine deposits over loamy till, occurs
on 0–3% slopes, and is somewhat poorly drained. The typical profile is: 0–28 cm
silt loam, 28–66 cm silty clay, and 66–152 cm gravelly loam. Average elevation is
442 m. Located in the USDA growing zone 6a (-23 °C to -21 °C minimum annual
temperature), this area has a mean annual precipitation of 91–122 cm, a mean annual
air temperature of 7–10 °C and a frost-free period of 115–195 days, with the
average first frost in mid-October and the average last frost in early to mid-May.
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Methods
New data for this study was taken from the LLP (http://www.lostladybug.org/),
the citizen-science project that documents changing distributions of coccinellids
across North America. At the time of this analysis, the LLP had over 17,000 verified
records of coccinellids, with over 1400 verified records from New York, and collection
has continued since then. LLP protocols direct that volunteers count groups
of aestivating coccinellids as single observations of that species because they may
not be functionally equivalent to a similar number of active individuals in the field.
We compared these data with published data from Pack (1925), Day (1965), and
Stephens (2002). Pack (1925) used visual sampling to survey Medicago sativa L.
(Alfalfa) fields in Ithaca, NY, in 1924; Day (1965) used sweep-net sampling to
survey Solanum tuberosum L. (Common Potato) fields in Riverhead, NY in 1956–
1958; and Stephens (2002) used yellow sticky-card sampling to survey in mixed
habitats (natural areas, gardens, and Alfalfa) in multiple locations in 2000–2001.
The LLP used visual and sweep-net sampling to survey in mixed habitats (natural
areas, gardens, wetlands, shorelines, buildings, agricultural crops—including Alfalfa,
Corn, Potato, Malus spp. (apple), Rubus idaeus L. (Raspberry)—in multiple
locations in 2008–2012.
We suspected that the major change reported in coccinellid complexes (Harmon
et al. 2007, Wheeler and Hoebeke 1995) was caused by the introduction of
two foreign species, Seven-Spotted Lady Beetle and Multicolored Asian Lady
Beetle. Thus, we examined each survey separately, and then pooled the two preintroduction
surveys—Pack (1925) and Day (1965)—and the two post-introduction
surveys— Stephens (2002) and the 2012 LLP effort—and compared the
pooled data as two distinct time periods with methods generally following Stephens
et al. (2012). To examine the diversity between pre- and post-introduction
time periods, we calculated Simpson’s D with the formula
D = Σ (n / N)2 ,
where n is the number of individuals in a category and N is the total number of all
coccinellids collected. To make the values more intuitive, we present 1 - D so that
low values represent lower diversity and higher values represent higher diversity.
Because pre-introduction surveys were done in single habitats and post-introduction
surveys covered multiple habitats, we also compared differences in the
diversity index in pre- and post-introduction surveys in a single crop, Alfalfa.
Because diversity indices are not directly quantitatively comparable, we compared
diversity between treatments by calculating and statistically comparing the
ratio of effective species (Jost 2006). The number of effective species (E) was
calculated as E = 1 / D. To determine the magnitude of the difference in the number
of effective species between time periods, we calculated the ratio of effective
species (E1 / E2) for each pair of treatments. Pairs with a ratio close to one have a
similar number of effective species, while values far from one denote pairs with
disparate numbers of effective species. To determine if pairs of treatments differed
significantly in their number of effective species we calculated the variance in the
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proportions (n / N) comprised by the species within a treatment using the formula
s2 = (R[*Σ(n / N)3] - Σ([n / N]2)2) / N,
where R = species richness, and then used those variances to perform a t-test.
Results
Among the 29 coccinellid species documented in the surveys (1924–present),
several species showed clear changes over time (Table 1). The two most notable
are the decrease in collection occurrence of four native species—Two-spotted Lady
Beetle, Nine-spotted Lady Beetle, Transverse Lady Beetle, and Convergent Lady
Beetle observed with the simultaneous increase in collection occurrence of three
exotic species—Seven-Spotted Lady Beetle, Multicolored Asian Lady Beetle, and
Fourteen-spotted Lady Beetle.
Of all species collected during the surveys, the native species, Transverse Lady
Beetle, showed one of the most marked declines. This was the most commonly collected
species in 1924 (ranked 1st) and accounted for 40.0% of the sample. Transverse
Lady Beetle represented only 5.0% of 1956–1958 collections, but was still
ranked 4th among all coccinellid species in abundance then. Because other studies
and surveys also show Transverse Lady Beetle was a constant but variable species
across the Northeast before introduction of exotic species, we combined the Pack
(1925) and Day (1965) data sets. Transverse Lady Beetle was not recorded in New
York in the 2000–2001 or 2008–2012 surveys.
Like Transverse Lady Beetle, Nine-spotted Lady Beetle was an important
component of the early surveys, accounting for 13.0% of the sample in 1924
(ranked 4th) and 18.0% between 1956 and 1958 (ranked 2nd). Nine-spotted Lady
Beetle was not found in the 2000-2001 survey but LLP surveyors rediscovered it
during the 2008–2012 survey where it represented 1.0% of collections (Table 1).
Specifically, in July and August 2011, volunteers and specialists working for the
LLP discovered over 20 adult Nine-spotted Lady Beetles on Long Island, NY.
All the individuals found were uniform with relatively large black spots on dark
red elytra (Fig. 1).
The results for Two-spotted Lady Beetle and Convergent Lady Beetle were very
similar to the pattern exhibited by Nine-spotted Lady Beetle. Two-spotted Lady
Beetle and Convergent Lady Beetle were not found in the 2000–2001 survey but
were rediscovered in the 2008–2012 survey, where they represented 0.2 and 0.3%
of collections, respectively (Table 1). However, unlike the Nine-spotted Lady Beetle,
which has only been found in one Long Island, NY, location, both Two-spotted
Lady Beetle and Convergent Lady Beetle have been found in multiple locations in
upstate NY as well as downstate. Starting in July 2009, volunteers and specialists
working for the LLP found Two Spotted Lady Beetles in a yard, public garden,
and park—all organically maintained—in Buffalo, Rochester, and Brooklyn, NY,
respectively. All the individuals found were uniform with two large black spots on
red elytra (Fig. 2). Starting in 2008, LLP personnel found Convergent Lady Beetles
in Woodside, Bayshore, Fairport, and Medina, NY.
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All three species—Two-spotted Lady Beetle, Nine-spotted Lady Beetle, and
Convergent Lady Beetle—were present in the early surveys, absent in the 2001–
2002 survey, and rediscovered in the 2008–2012 survey.
One native species, Coleomegilla maculata (Spotted Lady Beetle), revealed a
pattern inversely related to the other natives, representing 0.0% of the samples in
1924 and1956–1958, 19.0% in 2000–2001, and 12.0% in 2008–2012.
Three exotic species —Seven-Spotted Lady Beetle, Multicolored Asian Lady
Beetle, and Fourteen-spotted Lady Beetle—were not represented in the earliest
surveys because they had not yet become established in the US. By the 2000–2001
Table 1. Percentages and ranks (in parentheses) of native and introduced coccinellid species found in
four New York surveys conducted in various habitats between 1924 and 2012. * = introduced species.
Data source
Pack 1925 Day 1965 Stephens 2002 2012 LLP data
Crop Alfalfa Potatoes Mixed Mixed
Year sampled 1924 1956–1958 2000–2001 2008–2012
Species
Adalia bipunctata L. 2 (7) 3 (7) 0 0.2 (16)
Anatis labiculata (Say) 0 0 0 0.1 (18)
Anatis mali (Say) 0 0 0 0.3 (13)
Anisosticta bitriangularis (Say) 0 0 0 0.1 (21)
Brachiacantha indubitalis (Crotch) 0 0 16 (3) 0
Brachiacantha ursina (Fabricius) 0 0 15 (4) 0.2 (16)
Chilocorus kuwanae* Sylvestri 0 0 0 0.1 (21)
Chilocorus stigma (Say) 0 0 0 1 (6)
Coccinella novemnotata Herbst 13 (4) 18 (2) 0 1 (6)
Coccinella septempunctata* L. 0 0 1 (8) 8 (4)
Coccinella transversoguttata Brown 40 (1) 5 (4) 0 0
Coccinella trifasciata L. 11 (5) 2 (9) 0 1 (6)
Coccinella undecimpunctata* L. 0 52 (1) 0 0
Coleomegilla maculata DeGeer 0 0 19 (2) 12 (2)
Cycloneda munda Say 0 5 (4) 3 (6) 1 (6)
Diomus terminatus (Say) 0 3 (7) 0 0
Epilachna varivestis* Mulsant 0 0 0 0.2 (14)
Harmonia axyridis* (Pallas) 0 0 34 (1) 59 (1)
Hippodamia convergens Guerin 15 (2) 9 (3) 0 0.3 (12)
Hippodamia glacialis (Fabricius) 0 0 0 1 (6)
Hippodamia parenthesis (Say) 15 (2) 0 2 (7) 1 (6)
Hippodamia tredecimpunctata (L.) 3 (6) 4 (6) 0 0
Hippodamia variegata* (Goeze) 0 0 0 2 (5)
Hyperaspis binotata (Say) 0 0 0 0.1 (18)
Hyperaspis signata Olivier 0 0 0 0.1 (18)
Neoharmonia venusta (Melsheimer) 0 0 0 0.2 (14)
Olla v-nigrum (Mulsant) 0 0 0 0
Propylaea quatuordecimpunctata* L. 0 0 11 (5) 11 (3)
Psyllobora vigintimaculata (Say) 0 0 0 0.1 (21)
Total n 67 105 296 1458
Species richness 7 9 8 23
Simpson’s D 0.78 0.68 0.79 0.62
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Figure 1. The single individual that comprised the initial discovery in July 2011 of the first
Coccinella novemnotata (Nine-spotted Lady Beetle) seen in New York in 29 years.
Figure 2. The single individual
that comprised the initial discovery
in July 2009 of the first
Two-spotted Lady Beetle, Adalia
bipunctata, seen in New York
in 24 years.
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survey, these foreign species represented 46.0% of all species and they represented
78.0% of all species in the 2008–2012 survey. Multicolored Asian Lady Beetle was
the most common species in both of the recent surveys.
One exotic species exhibited a different pattern: Coccinella undecimpunctata
(Eleven-spotted Lady Beetle) represented 52.0% of the surveyed population between
1956 and 1958 but did not occur in any other of the three surveys.
Table 2. Comparison of coccinellid complexes in pooled New York surveys, pre- and post-introduction
of three exotic coccinellid species: Coccinella septempunctata, Harmonia axyridis, and Propylaea
quaturodecimpunctata. Differences between numbers of effective species and between percent
of introduced species were compared using t-tests (P < 0.05).
Pre-introduction Post-introduction
(Pack 1925, Day 1965) (Stephens 2001; 2012 LLP data)
Total individuals (N) 165 1755
Species richness (S) 9 26
Diversity index (1 - D) 0.82 0.67
Effective species (E) 5.4a 3.0b
Percent introduced species 33%a 74%b
Figure 3. Map of all lady beetle observations in New York by the Lost Ladybug Project
2008–2012 with introduced species in red, and native species C. novemnotata in green, A.
bipunctata in yellow, and all other native species in blue.
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The diversity indices for the four surveys ranged from 0.79 to 0.62, with each
period (pre- and post-establishment of major foreign species) having one relatively
high and one lower diversity rating (Table 1). The pooled pre-introduction
surveys had a higher diversity index (0.82) than the pooled surveys from the postintroduction
time period (0.67) even though species richness was lower (9 and 26,
respectively; Table 2). When we compared post- and pre-introduction-periods collections
from a single crop, the diversity index for coccinellids surveyed in Alfalfa
in 2001 (0.65; Stephens 2002) was substantially lower than the index for coccinellids
surveyed in 1924 (0.78; Pack 1925).
Differences in this or any diversity index can be difficult to interpret, but the
number of effective species (E) in the pre-introduction period (5.4) was also significantly
higher than the number in the post-introduction period (3.0; P < 0.001;
Table 2) with a pre- to post-introduction ratio of 0.55 for effective species. This
decrease in the number of effective species corresponded with a significant increase
of the dominance of foreign species, which increased from 33.0% in the pre-introduction
time period to 74.0% in the post-introduction period (P = 0.001; Table 2).
Results from the LLP’s 2008–2012 survey added to our knowledge about
the current status of the coccinellid complex in NY (Fig. 3). Our data show
that the coccinellid complex in NY is composed of 78% foreign ladybugs, dominated
by Multicolored Asian Lady Beetle, and 22% native ladybugs, dominated
by Spotted Lady Beetle; we detected native Two-spotted Lady Beetle and Ninespotted
Lady Beetle only rarely.
Discussion
One of the major patterns in the coccinellid complex in NY has been the disappearance
and rediscovery of several native species. These species were present and,
in many cases, they were substantial components of the coccinellid complex of New
York up to 50 years ago, but by 2000 they were notably absent. Using the Cornell
University Insect Collection (CUIC), it was possible to determine more precisely
when these species were last seen in New York within the period 1958–2000. The
latest dated specimens in the CUIC were 1980, 1982, and 1985 for Transverse Lady
Beetle, Nine-spotted Lady Beetle, and Two-spotted Lady Beetle, respectively. The
same pattern of disappearance has been shown across the Northeast. The most recent
survey of northeastern North America to detect Nine-spotted Lady Beetle was
in 1982, and 6 subsequent surveys from 1993 to 2001 in various northeastern states
and provinces did not record this species (Losey et al. 2007).
Some native species have disappeared and have not yet been rediscovered. Despite
a multi-location survey in 2001 and extensive sampling by LLP volunteers
across NY—including over 1400 coccinellids documented from 2008–2012—
Transverse Lady Beetle, has not been rediscovered in NY. The same is true for the
Northeast as a whole; other research studies document that Transverse Lady Beetle
was a common but variable species in the Northeast prior to the introduction of
exotic coccinellid species. For example, during 1942–1971 in Maine potato fields,
Transverse Lady Beetle ranged in percent of the total coccinellid population from
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5.7 to 66.0 (Shands et al. 1972), and Storch (1973) referred to Transverse Lady
Beetle as usually the most abundant predator in Maine Potato fields. Yet from
2008–2012, no Transverse Lady Beetles have been found by LLP volunteers in
Maine or any other northeastern state. Based on the surveys we examined, it appears
that at least one other species has disappeared from New York as well. Although we
know very little about its relative abundance, the CUIC has collection records of
Coccinella hieroglyphica L. (Hieroglyphic Lady Beetle) from as late as 1949, but
we did not observe it during our surveys.
Although the patterns are clear, it is not possible to determine if species like
Nine-spotted Lady Beetle and Two-spotted Lady Beetle were extirpated from New
York for a period of time between their last collection and then they were rediscovered
between 2008–2012 by the LLP or if they were always present at a low
density but were just not detected by interim surveys. The latter seems more likely
based on 1) both species still appearing to be at low enough densities that they
could easily have been missed, 2) the relatively small geographic area covered by
the 2000–2001 survey, and 3) the low level of sampling in the Lake Ontario coastal
region, where Two-spotted Lady Beetle was rediscovered, and the Long Island region
where Nine-spotted Lady Beetle was rediscovered. The type of small, widely
dispersed volunteer surveys employed by the LLP has been shown to be more effective
at detecting rare species than more concentrated surveys (Losey et al. 2012a).
Participants in the LLP surveyed a wide variety of locations across New York, and
the breadth of these surveys resulted in the rediscovery of the two rare native species
(Fig. 3).
Several hypotheses have been proposed to explain the decline of native coccinellid
species in the Northeast, and most encompass negative interactions with introduced
coccinellid species. Wheeler and Hoebeke (1995) were among the first to point out
the coincidence of the decline of the native Nine-spotted Lady Beetle with the establishment
and spread of non-native Seven-Spotted Lady Beetle. A more recent study
demonstrated a decrease in the average body size of recently field-collected Ninespotted
Lady Beetles compared to historical specimens across multiple geographical
locations and a broad time period (Losey et al. 2012b). This finding is consistent
with the hypothesis that foreign species are outcompeting native species for prey. An
earlier study found no decline in body size in five other native species and suggested
that IGP or habitat compression might be causing the decline of these native coccinellid
species (Evans 2000). However, the study occurred in a single geographical crop
location, over a much shorter time-span than Losey et al. (2012b), and most importantly,
Nine-spotted Lady Beetle was not included because it occurred in insufficient
numbers (E. Evans, Utah State University, Logan, UT, pers. comm.). Although further
studies of historical records and additional geographically wide field surveys are
needed on other native species to further understand the role of competition for prey in
their overall decline, it appears that foreign species are at least playing some role, and
perhaps a variety of roles, in the decline of native species.
Another interesting finding may, upon further study, help to explain the decline
of native coccinellid species in the Northeast. In contrast to the Nine-spotted Lady
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Beetles submitted to the LLP by citizen scientists from western states, which were
variable and often dominated by individuals with very small black spots on peach
or adobe colored elytra, all the individuals found in NY were uniform with relatively
large black spots on dark red elytra. Similarly, all the individuals of Two-spotted
Lady Beetle found in NY were uniform with two large black spots on red elytra,
while other populations contain individuals with no spots, four spots, and a reverse
or melanic form. Further study may reveal that specific differences in these and
other traits are linked to differences in survival. Differences in coccinellid coloration
have been linked to variation in several chemical compounds and subsequent
defense against predation by birds (Blount et al. 2012). Differences in coccinellid
spot size or melanized surface area have been linked to differences in fitness and to
changes in climate (de Jong and Brakefield 1998).
It is important to note that several species are not following the patterns in
population changes described above. Notably Spotted Lady Beetle is a native species
that is thriving and perhaps even increasing its relative density. One possible
explanation for the continuous survival of Spotted Lady Beetle is that it is facultatively
pollenivorous, while most other species in the coccinellinae are obligate
predators (Michaud and Grant 2005). No such obvious explanation presents itself
for Eleven-spotted Lady Beetle (Wheeler and Hoebeke 2008). This was the most
common species found in the 1956–1958 survey, but it was not seen in our surveys,
although there is one 1982 specimen at CUIC. It seems plausible that conditions
allowed this foreign species to flourish for a time—it was first documented in the
region in 1912 (Gordon 1985)—but then something changed in the environment
that resulted in population decreases (Baltz and Moyle 1993).
Beyond individual species, it is important to consider patterns for the coccinellid
complex as a whole. From our calculations of Simpson’s diversity index,
it does not appear that there is a substantial difference in diversity between the
pre-introduction surveys (1924 and 1956–58) and the post-introduction surveys
(2001 and 2008–2012; see Table 1). However, one difference between the pre- and
post-introduction survey protocols may serve to mask an important pattern. Both
pre-introduction surveys were conducted in a single type of habitat, but the postintroduction
surveys were conducted across multiple habitats. This is likely an
important factor because coccinellid complexes differ across habitats, so combining
habitats may obscure the actual diversity of a specific habitat and how it has
changed over time. The 2000–2001 survey explains this phenomenon. We conducted
our survey across three habitats: natural areas, gardens, and Alfalfa fields.
The pooled diversity index, 0.80, is substantially higher than the averaged diversity
index calculated using the index value for each specific habitat (0.71). Because the
2000–2001 and 1956–1958 surveys included Alfalfa, it was possible to compare
diversity between pre- and post-introduction populations in a single habitat. The
result supports our overall conclusion that species diversity has declined with the
introduction of coccinellids and the subsequent decline of nati ve species.
To further elucidate the differences between pre- and post-introduction coccinellid
complexes, we can pool the two pre-introduction surveys and compare
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2014 Vol. 21, No. 2
them to the two post-introduction surveys. The results of this comparison show
some important differences between the two complexes (Table 2). First, we have
many more samples from the post-introduction era (1755) compared to the preintroduction
era (165). This higher level of sampling likely contributed to greater
species richness in the post-introduction complex compared to the pre-introduction
complex. Even with the greater species richness, the diversity index for the postintroduction
complex is substantially lower than the index for the pre-introduction
complex. Although diversity indices give a useful single measure of diversity, it can
be difficult to interpret differences between diversity indices across space or time
(Jost 2006). One practical alternative is to calculate effective species (Jost 2006).
This method yields a value that is directly and statistically comparable between
two time periods. One useful way to interpret these values is to assess the ratio
of the number of effective species across two sets of conditions. A ratio close to 1
indicates very similar diversity, and ratios far from 1 indicate major differences in
diversity. Our pre- and post-introduction numbers of effective species yield a ratio
of 0.55, which indicates New York has lost nearly half of the diversity in its coccinellid
complex following the introduction of major foreign species. We suspect this
lowered diversity has been caused by the measurable increase in the dominance of
foreign coccinellid species.
The decline of native coccinellid species in New York over the last several
decades is cause for concern, particularly because a diverse complex of coccinellids
that includes native species has been shown to provide the most effective pest
suppression (Snyder 2009). However, recent rediscoveries have demonstrated that
although many of the native species have become rare, they are not extirpated in
New York. The confirmation of these species in the same locations over several
seasons offers hope that they are viable populations that may persist and potentially
even expand to provide more balance with introduced species. Long-term citizenscience
surveys such as the LLP are particularly well suited to provide the type of
data needed to monitor these changes. Beyond determining the impact on coccinellid
species themselves, this system can serve as a model for predicting the impact
of other invasive species on the natural history of the Northeast.
Acknowledgments
The authors wish to thank the Quail Hill Farm 2011–2013 field crews for their enthusiastic
assistance. The authors also thank the Peconic Land Trust for their gracious hospitality
and support. The LLP is funded by a grant from the Informal Science Education Program of
the National Science Foundation.
Literature Cited
Angalet, G., and R. Jacques. 1973. USDA. Cooperative economic insect report. Newark,
DE. 883–884 pp.
Baltz, D.M., and P.B. Moyle. 1993. Invasion resistance to introduced species by a native
assemblage of California stream fishes. Ecological Applications 3:246–255.
Northeastern Naturalist Vol. 21, No. 2
J.E. Losey, L.L. Allee, E. Stephens, R.R. Smyth, P. Priolo, L. Tyrrell, S. Chaskey, and L. Stellwag
2014
283
Bazzocchi, G.G., A. Lanzoni, G. Accinelli, and G. Burgio. 2004. Overwintering, phenology,
and fecundity of Harmonia axyridis in comparison with native coccinellid species
in Italy. BioControl 49:245–260.
Blount J., H. Rowland, F. Drijfhout, J. Endler, R. Inger, J. Sloggett, G. Hurst, D. Hodgson,
and M. Speed. 2012. How the ladybird got its spots: Effects of resource limitation on
the honesty of aposematic signals. Functional Ecology 26:1–9.
Cottrell, T.E., and K.V. Yeargan. 1998. Intraguild predation between an introduced lady
beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla
maculata (Coleoptera: Coccinellidae). Journal of the Kansas Entomological
Society 71:159–163.
Day, W.H. 1965. The identification and importance of biotic and abiotic factors affecting
aphids on Long Island potatoes. Ph.D. Thesis. Cornell University, Ithaca, NY. 420 pp.
de Jong, P.W., and P.M. Brakefield. 1998. Climate and change in clines for melanism in
the Two-Spot Ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Proceedings:
Biological Sciences 265:39–43.
Elliot, N., R. Kieckhefer, and W. Kauffman. 1996. Effects of an invading coccinellid on
native coccinellids in an agricultural landscape. Oecologia 105:537–544.
Evans, E.W. 2000. Morphology of invasion: Body-size patterns associated with establishment
of Coccinella septempunctata (Coleoptera: Coccinellidae) in western North
America. European Journal of Entomology 97:469–474.
Gagnon, A.E., G.E. Heimpel, and J. Brodeur. 2011. The ubiquity of intraguild predation
among predatory arthropods. PLoS ONE 6:e28061.
Gardiner, M.M., M.E. O'Neal, and D.A. Landis. 2011. Intraguild predation and native lady
beetle decline. PLoS ONE 6:e23576.
Gordon, R.D. 1985. The Coccinellidae (Coleoptera) of America North of Mexico. Journal
of the New York Entomological Society 93:1–912.
Gordon, R.D., and N. Vandenberg. 1991. Field guide to recently introduced species of Coccinellidae
(Coleoptera) in North America, with a revised key to North American genera
of Coccinellini. Proceedings of the Entomological Society of Washington 93:845–864.
Harmon, J.E., J. Stephens, and J. Losey. 2007. The decline of native coccinellids (Coleoptera:
Coccinellidae) in the United States and Canada. Journal of Insect Conservation
11:85–84.
Hodek, I., A. Honek, and H.F. van Emden. 2012. Ecology and Behavior of the Ladybird
Beetles (Coccinellidae). Wiley-Blackwell, New York, NY. 600 pp.
Iperti, G. 1999. Biodiversity of predaceous coccinellidae in relation to bioindication and
economic importance. Agriculture, Ecosystems and the Environment 74:323–342.
Jost, L. 2006. Entropy and diversity. Oikos 113:363–375.
Losey, J., J. Perlman, and E. Richard Hoebeke. 2007. Citizen scientist rediscovers rare
Nine-spotted Lady Beetle, Coccinella novemnotata, in eastern North America. Journal
of Insect Conservation 11:415–417.
Losey, J.E., L. Allee, and R. Smyth. 2012a. The Lost Ladybug Project: Citizen spotting
surpasses scientist’s surveys. American Entomologist 58:22–24.
Losey, J., J. Perlman, J. Kopco, S. Ramsey, L. Hesler, E. Evans, L. Allee, and R. Smyth.
2012b. Potential causes and consequences of decreased body size in field populations of
Coccinella novemnotata. Biological Control 61:98–103.
Metcalf, R.L., and W.H. Luckman. 1994. Introduction to Insect Pest Management. Wiley,
New York, NY. 650 pp.
Northeastern Naturalist
284
J.E. Losey, L.L. Allee, E. Stephens, R.R. Smyth, P. Priolo, L. Tyrrell, S. Chaskey, and L. Stellwag
2014 Vol. 21, No. 2
Michaud, J.P., and A.K. Grant. 2005. Suitability of pollen sources for the development and
reproduction of Coleomegilla maculata (Coleoptera: Coccinellidae) under simulated
drought conditions. Biological Control 32:363–370.
New York State Department of Environmental Conservation (NY DEC). No date. Natural
history of New York State. p. 20. Available online at http://www.dec.ny.gov/docs/wildlife_
pdf/nathist.pdf. Accessed May 2014.
Obrycki, J.J., K.L. Giles, and A.M. Ormord. 1998. Interactions between an introduced and
an indigenous coccinellid species at different prey densities. Oecologia 117:279–285.
Obrycki, J.J., N.C. Elliot, and L.G. Giles. 2000. Coccinellid introductions: Potential for
and evaluation of nontarget effects. Pp. 127–145, In P.A. Follett and J.J. Duan (Eds.).
Nontarget Effects of Biological Control Introductions. Kluwer Academic Publishers,
Norwell, MA. 316 pp.
Pack, H.J. 1925. A biological study of certain ladybird beetles (Coccinellidae). Ph.D. Dissertation.
Cornell University, Ithaca, NY. 157 pp.
Shands, W.A., G.W. Simpson, H.E. Wave, and C.C. Gordon. 1972. Importance of arthropod
predators in controlling aphids on Potatoes in northeastern Maine. Life Sciences and
Agriculture Experiment Station Technical Bulletin 54. 49 pp.
Snyder, W. 2009. Coccinellids in diverse communities: Which niche fits? Biological Control
51:323–335.
Stephens, E.J. 2002. Apparent extirpation of Coccinella novemnotata in New York State:
Optimizing sampling methods and evaluating explanations for decline. M.Sc. Thesis.
Cornell University, Ithaca, NY. 63 pp.
Stephens, E.J., J.E. Losey, L. Allee, A. DiTommaso, C. Bodner, and A. Breyre. 2012. The
impact of Cry 3Bb1 Bt-maize on two guilds of beneficial beetles. Agriculture, Ecosystems
and Environment 156:72–81.
Storch, R.H. 1973. The effect of photoperiod on Coccinella transversoguttata
(Coleoptera:Coccinellidae). Entomologia Experimentalis et Applicata 16:77–82.
Vilcinskas, A., K. Stoecker, H. Schmidtberg, C.R. Röhrich, and H. Vogel. 2013. Invasive
Harlequin Ladybird carries biological weapons against native competitors. Science
340:862–863.
Wheeler, A.G., Jr., and E.R. Hoebeke. 1995. Coccinella novemnotata in northeastern North
America: Historical occurrence and current status (Coleoptera: Coccinellidae). Proceedings
of the Entomological Society of Washington 97:701–716.
Wheeler, A.G., Jr., and E.R. Hoebeke. 2008. Rise and fall of an immigrant lady beetle:
Is Coccinella undecimpunctata L. (Coleoptera: Coccinellidae) still present in North
America? Proceedings of the Entomological Society of Washington 110:817–823.