oidea: Notodontidae) Parts 1 and 2: Josiini. Bulletin of the American
Museum of Natural History.
Miller, J. S. and P. Thiaucourt. 2011. Diversity of prominent moths (Lepidoptera: Noctuoidea: Notodontidae) in the cloud forests of northeastern
Ecuador, with descriptions of 27 new species. Annals of the Entomological Society of America. In press.
Pearson, C. V., T. J. Massad, and L. A. Dyer. 2008. Diversity cascades in
alfalfa fields: From plant quality to agroecosystem diversity. Environmental Entomology 37:947-955.
Richards, L. A., L. A. Dyer, A. M. Smilanich, and C. D. Dodson. 2010.
Synergistic effects of amides from two Piper species on generalist and
specialist herbivores. Journal of Chemical Ecology 36:1105-1113.
Rodríguez-Castañeda, G., L. A. Dyer, G. Brehm, H. Connahs, R. E. Forkner,
and T. R. Walla. 2010. Tropical forests are not flat: how mountains affect
herbivore diversity. Ecology Letters 13:1348-1357.
Smilanich, A. M., L. A. Dyer, J. Q. Chambers, and M. D. Bowers. 2009.
Immunological cost of chemical defence and the evolution of herbivore
diet breadth. Ecology Letters 12:612-621.
Stireman, J. O., L. A. Dyer, D. H. Janzen, M. S. Singer, J. T. Li, R. J. Marquis,
R. E. Ricklefs, G. L. Gentry, W. Hallwachs, P. D. Coley, J. A. Barone, H. F.
Greeney, H. Connahs, P. Barbosa, H. C. Morais, and I. R. Diniz. 2005.
Climatic unpredictability and parasitism of caterpillars: Implications
of global warming. Proceedings of the National Academy of Sciences of
the United States of America 102:17384-17387.
Wagner, D. L., D. F. Schweitzer, J. B. Sullivan, and R. C. Reardon. 2011.
Owlet Caterpillars of Eastern North America. Princeton University
Press. 576 pp. In press.
Lee A. Dyer, Angela M. Smilanich, faculty, Department of Biology, University
of Nevada, Reno, NV. David L. Wagner, faculty, Department of Ecology
and Evolutionary Biology, University of Connecticut, Storrs, CT. Harold F.
Greeney, scientific director, Yanayacu Biological Station & Center for Creative
Studies, Cosanga, Napo, Ecuador. Tara J. Massad, postdoctoral researcher,
Max Planck Institute for Biogeochemistry, Jena, Germany. Moria L. Robinson,
recent graduate, Department of Biology, Middlebury College, Middlebury, VT.
Mark S. Fox, and Rebecca F. Hazen, Ph.D. students, Department of Ecology
and Evolutionary Biology, Tulane University, New Orleans, LA. Andrea E.
Glassmire, and Nicholas A. Pardikes, Ph.D. students, Department of Biology, University of Nevada, Reno, NV. Kirsha B. Fredrickson, undergraduate
student, Department of Biology, University of Nevada, Reno, NV. Clark V.
Pearson, Ph.D., Department of Ecology and Evolutionary Biology, Tulane
University, New Orleans, LA. Grant Gentry, faculty, Department of Biology,
Samford University, Birmingham, AL. John O. Stireman III, faculty, Department of Biological Sciences, Wright State University, Dayton, OH.
Instant symposiuM
Tachinid Flies and Monarch Butterflies:
Citizen Scientists Document Parasitism Patterns over
Broad Spatial and Temporal Scales
Karen Oberhauser
T
he Tachinidae represent the largest family of dipteran
parasitoids, with ~10,000 species. Most of their hosts are
Lepidoptera, and it is generally assumed that tachinid flies
have wide host ranges (i.e., many suitable host species) (Stireman
et al. 2006). However, it is likely that tachinid host ranges have been
overestimated; in a long-term study of tachinid flies reared from hosts
collected in Costa Rica, many species that appeared to be generalists
were shown to be host-specific cryptic species (Smith et al. 2007).
Lespesia archippivora (Riley) (Tachinidae) has been reported to
parasitize larvae of 25 Lepidoptera species in 14 families, and one
species of Hymenoptera (Arnaud 1978). It is widespread throughout
North and Central America, has been found in Brazil (Arnaud 1978),
and was introduced into Hawaii for biocontrol in 1898 (Etchegaray
and Nishida 1975). Except for its occurrence in multi-host speciesrearing projects, L. archippivora has only been studied in detail in
monarchs (Danaus plexippus L.) and beet armyworms (Spodoptera
exigua Huber). It parasitizes monarch larvae in the continental U.S.
and Hawaii (Etchegaray and Nishida 1975, Prysby 2004, Oberhauser
et al. 2007), with one long-term, broad-scale monitoring project
American Entomologist  •  Volume 58, Number 1
documenting an overall parasitism rate of ~13% (Oberhauser et al.
2007). In the southern U.S., the beet armyworm is reported to be a
preferred L. archippivora host (Stapel et al. 1997).
North American monarchs complete multiple generations on their
milkweed host plants (Asclepias spp.) within a summer breeding
season, and overwinter in central Mexico (eastern migratory population) or coastal California (western migratory population). They
remain in their wintering sites in a state of reproductive diapause
from early November through mid-March, before returning to their
spring breeding grounds. In the east, returning migrants lay eggs
in the southeastern U.S. (Texas to Florida and Oklahoma to North
Carolina) and their offspring recolonize the summer breeding range
(roughly the northeastern quarter of the U.S. and southern Ontario
and Quebec), where they undergo two to three non-migratory generations before the final generation returns to Mexico. There is some
fall breeding by southward migrants in the southern U.S., resulting
in another generation that presumably migrates to Mexico. Although
some monarchs remain throughout the winter in the southern U.S.,
where at least some of them continue to breed (Prysby & Oberhauser
19
2004), tagging records and host plant fingerprint studies suggest
that the vast majority of northern monarchs that eclose after midto late August migrate to Mexico. The smaller western population
undergoes a shorter migration between breeding ranges west of the
Rocky Mountains and coastal California.
Immature monarchs have a large suite of invertebrate predators, with approximately 92% mortality during the egg and early
larval stages (Prysby 2004 and references therein). Twelve species
of tachinid flies, at least one braconid wasp (Arnaud 1978), and a
pteromalid wasp (Pteromalus puparum L., personal observation)
have been reported in monarchs. However, many of these may represent incidental or very rare parasitism events.
Here, I report the results of an ongoing study that utilizes data
collected by citizen scientists in the Monarch Larva Monitoring
Project (MLMP, www.mlmp.org). I document long-term patterns in
parasitism of monarchs by L. archippivora, including relationships
between monarch density and L. archippivora parasitism rates.
Methods
Volunteer citizen scientists in the MLMP have documented temporal and spatial variation in monarch egg and larval abundances
since 1997. Their monitoring sites include gardens, railroad rightof-ways, roadsides, abandoned fields and pastures, natural habitats,
and restored prairies (see Prysby and Oberhauser 2004 for details).
In this study, I used two types of MLMP data. First, volunteers estimate weekly monarch density per milkweed ramet1 by checking tens
to hundreds of ramets and noting the number of monarch eggs and
larvae observed. They enter these data into an online data repository.
Second, from 1999-2011, a subset of MLMP volunteers have collected
thousands of monarch larvae to measure tachinid parasitism rates.
Most volunteers collect and rear 4th or 5th instars, but have contributed records from hundreds of monarchs collected as eggs and
younger larvae. They rear them in their homes, recording the date,
location, and larval stadium at collection, as well as the outcome of
each rearing (adult monarch; died of unknown cause; died accidental
death; parasitized by fly; parasitized by wasp). A “notes” data field
allows volunteers to record additional information that they consider
relevant. Most also record the number of parasitoids that emerge from
each host. Volunteers only identify parasitoids to order, but all of the
flies that we have identified to species (several dozen from throughout
the U.S.) have been L. archippivora (Oberhauser et al. 2007).
For the analyses reported here, I omitted data when monarch
death was accidental (e.g., dropping the specimen; crushing between
the lid and rearing container). I also omitted data from a volunteer
who did not understand the data entry protocol and entered data for
more than one monarch in a single entry, and another whose reared
larvae suffered very high rates (47%) of mortality.
To compare rates of tachinid fly parasitism to monarch densities, I calculated regional metrics of immature monarch density collected by MLMP volunteers, using data from the upper midwestern
(MN, WI, IA, and MI) and southern (TX, OK, MS, AL, NC, SC, GA, FL)
United States. I used egg density (eggs observed/ramets examined)
throughout a given region in a given week to represent monarch
density during that week. In the upper Midwest, I used the July or
August week with peak density to represent annual population size.
1
Because many individual Asclepias plants, especially A. syriaca (the most commonly used species in the northeastern quarter of the U.S.), produce multiple ramets
from a single plant, or genet, individual milkweed stems, regardless of species, are
referred to as ramets throughout this paper.
20
In the South, I calculated two maxima for each region: one during
the spring migration (April through mid-May) and another during
the fall migration (September and October). Monarchs are generally
absent from this region for most of June–August. I only used data
from weeks during which >100 ramets were examined from at least
two sites, and did not use data from years in which this criterion was
met for fewer than five and six weeks in the spring and fall in the
South, respectively. All years of the study had well over 100 observed
plants during all July and August weeks in the upper Midwest. These
criteria made it more likely that I used true maxima to represent
annual monarch densities.
I calculated the marginal rate of parasitism in each larval stadium
as:
mit = 1 – (1 – qi)qit/qi
where qit = the apparent mortality from tachinid parasitism of larvae
collected during stadium i, and qi = the mortality from all combined
causes during stadium i (modified from Bellows et al. 1992). This is
appropriate because larvae that died from other causes may have
been parasitized (in fact, dissections suggest that parasitism often
results in host death before the parasitoids mature [personal observations and Ilse Gebhard, personal communication]). Using the
marginal rate corrects for the fact that the measured rate of parasitism is likely to underestimate the actual rate.
I estimated the daily risk of parasitism in each stadium (Ri), correcting for time in each stadium and the relative abundance of each
stadium. These calculations assume that both parasitoids and MLMP
volunteers encounter monarchs in proportion to their abundance.
I estimated relative abundance using MLMP data that met the following criteria: volunteers monitored at least four times during a
given year (to eliminate year/site combinations in which volunteers
may have missed stages due to monarch phenology); volunteers
monitored 10 or more plants per monitoring event (to decrease
sampling error); volunteers did not report more larvae than eggs;
and volunteers reported at least some eggs (volunteers not meeting
the latter two categories probably missed monarchs that were less
apparent, such as eggs and earlier stadia). I used the following formula to estimate the relative daily risk of parasitism in each stadium:
Ri = [(mit – m(i-1)t)/t is i],
where mit is defined above, ti = the number of days spent in stadium i
and si = survival to stadium i from i=1. Monarchs spend approximately
2 days as 1st–4th instars and 4 days as 5th instars; si is calculated as
N i /N1, where N i= total number of larvae in stadium i observed by
MLMP volunteers.
Results
Data from 130 volunteers who reared 1–996 eggs and larvae over
the 13 years of the study (Fig. 1) provided 7,686 usable records. I
used all of these records to study rates of parasitism during different
stages. To look at annual variation in parasitism rates, I only used
data from larvae collected in the fifth (and final) stadium because
parasitism rates increase with the age of monarch at collection (see
below). I also limited this analysis to years in which parasitism data
from over 10 fifth-instar monarchs were reported in the region of
study; this criterion was met every year from 2000-2010 in the upper
Midwest (range 87-377, mean = 204) and in eight of these 11 years
in the South (range 10-461, mean = 125).
American Entomologist  • Spring 2012
Fig. 1. Frequency distribution of the number of monarchs reared by individual volunteers from 1999-2011 (note that 2011 data are incomplete).
Volunteers collected and reared monarchs in all immature stages
(N: egg = 654, L1 = 619, L2 = 417, L3 = 493, L4 = 1458, L5 = 3999,
pupa = 46). From one to 12 flies emerged from individual monarchs.
Later stages tended to produce more flies per monarch, although this
relationship is only statistically significant when comparing 1st–3rd to
4th–5th instars (Fig. 2). Monarchs collected during later stadia were
more likely to be parasitized and the daily risk of parasitism was
higher during the middle three stadia (Fig. 3).
There is a correlation between tachinid parasitism rates and
monarch population densities in the upper Midwest the previous
year (Fig. 4; Pearson coefficient = 0.663, N = 11, p = 0.0262). There
is no relationship between tachinid parasitism rates and current-year
monarch densities in the upper Midwest, nor between parasitism and
spring or fall monarch densities during the current or previous year
in the southern U.S.
Fig. 2. Number of flies that emerged from monarchs collected during
different larval stadia (with standard error). Kruskal-Wallis One-Way AOV
statistic for stadia considered individually = 11.83, p = 0.066; for combined 1st-3rd and 4th-5th K-W statistic = 6.80, p = 0.0091. Note extremely
variable sample sizes.
Fig. 3. Marginal parasitism risk of monarchs collected during each larval
stadium (solid bars) and the daily risk of parasitism (open bars). The
daily risk of parasitism for pupae was not calculated, since it is assumed
that the higher parasitism rate for pupae is due to parasitism occurring
late during the fifth stadium. See text for calculation details.
In the upper Midwest, high monarch densities one year are followed by high L. archippivora parasitism rates in the next year. One
explanation for this coupling is that monarchs drive L. archippivora
numbers. This hypothesis seems contrary to the assumption that L.
archippivora is a generalist, but could result if L. archippivora identified from different hosts are actually host races or cryptic species, or if
monarchs are the primary L. archippivora host and other host species
represent spill-over parasitism. Alternatively, the coupling may not
be causal, and could result if multiple L. archippivora hosts follow
similar cycles, perhaps tracking abiotic conditions. The hypothesis
that monarchs are the primary L. archippivora host is supported by
Janzen and Hallwachs’ (2009) extensive caterpillar-rearing study in
Costa Rica, in which all of 27 rearings of L. archippivora were from
monarchs (out of 292 monarch rearings and 51,425 total rearings).
Monarch migratory patterns in the eastern U.S. result in temporally separated spring and fall generations in the South, and continuous summer generations in the North (Prysby and Oberhauser
2004). Unless the parasitoids undergo summer diapause, they must
use alternate hosts during the summer in the southern U.S. Thus,
phenological overlap between monarchs and L. archippivora may
differ throughout the breeding range in ways that could affect L. archippivora specificity. The fact that the correlation between monarch
densities and parasitism rates the following year was only found in
the upper Midwest supports the hypothesis that the L. archippivora
/monarch interaction is more specific in this region, as does the fact
that Stireman and Singer (2003) reared L. archippivora from five
Discussion
These findings confirm the conclusion that dipteran parasitoids
comprise an important source of biotic mortality for monarch larvae
(Oberhauser et al. 2007). Much of this mortality is initiated after the
egg and first stadium, periods during which most monarchs are killed
by other natural enemies (Prysby 2004, personal observations).
While tachinid flies parasitize monarchs as first or fifth instars,
their daily risk of parasitism is lower than in the middle three stadia.
Further study could help determine whether these larvae are less
likely to be encountered by the flies, or simply less attractive once
they’re encountered.
American Entomologist • Volume 58, Number 1
Fig. 4. Upper Midwestern monarch density in year t-1 (peak July-August
monarch eggs/milkweed ramet) and proportion of 5th-instar monarch
larvae that were parasitized by L. archippivora.
21
other hosts in the southwestern U.S.
This research demonstrates the value of detailed and long-term
records on host distribution and abundance as well as parasitism
rates that have been collected by MLMP volunteers. A study of this
magnitude would have been impossible without their contributions.
Acknowledgments
I thank the hundreds of MLMP volunteers who have contributed
to this project, especially Deb Marcinski, Emily Toriani-Moura,
Alan Williams, Donna Kemp, Brian Bockhahn, Sondra Cabell,
Ilse Gebhard, Sharon Duerkop, Darlene Pinchot, Susan Payant,
Suzanne Oberhauser, Diane Rock, and Charlie Cameron; and
Monarch Lab students and staff for their help in developing
protocols and communicating with volunteers. This research was
supported by the National Science Foundation (ESI 9731429,
ESI 0104600), the National Center for Ecological Analysis and
Synthesis, and the Monarchs in the Classroom program at the
University of Minnesota.
Literature Cited
Arnaud, P.H. 1978. A host-parasite catalog of North American Tachinidae
(Diptera). (Administration SaE, ed.): USDA 860.
Bellows Jr., T.S., R.G. Van Driesche, J.S. Elkinton. 1992. Life-table construction and analysis in the evaluation of natural enemies. Annu. Rev.
Entomol. 37: 587–614.
Etchegaray, J.B., T. Nishida. 1975. Biology of Lespesia archippivora (Diptera: Tachinidae). Proc. Haw. Entom. Soc. 12: 41-49.
Janzen, D.H., W. Hallwachs. 2009. Dynamic database for an inventory of
the macrocaterpillar fauna, and its food plants and parasitoids, of Area
de Conservacion Guanacaste (ACG), northwestern Costa Rica. (http://
janzen.sas.upenn.edu)
Oberhauser, K.S., I. Gebhard, C. Cameron, S. Oberhauser. 2007. Parasitism of monarch butterflies (Danaus plexippus) by Lespesia archippivora
(Diptera: Tachinidae). Amer. Midl. Nat. 157: 312-328.
Prysby, M.D. 2004. Natural enemies and survival of monarch eggs
and larvae, pp. 27-37. In The Monarch Butterfly: Biology and Conservation. Oberhauser, K.S., M.J. Solensky, eds. Ithaca, NY: Cornell
University Press.
Prysby, M., K. Oberhauser. 2004. Temporal and geographical variation
in monarch densities: Citizen scientists document monarch population
patterns, pp. 9-20. In The Monarch Butterfly: Biology and Conservation.
Oberhauser, K.S., M.J. Solensky, eds. Ithaca, NY: Cornell University Press.
Smith, A.M., D.M. Wood, D.L. Janzen, W. Hallawachs, P.D.N. Hebert. 2007.
DNA barcodes affirm that 16 species of apparently generalist tropical
parasitoid flies (Diptera, Tachinidae) are not all generalists. Proc. Nat.
Acad. Sci. 104: 4967-4972.
Stapel J.O., J.R. Ruberson, H.R. Gross Jr., W.J. Lewis. 1997. Progeny allocation by the parasitoid Lespesia archippivora (Diptera: Tachinidae)
in larvae of Spodoptera exigua (Lepidoptera: Noctuidae). Environ.
Entomol. 26: 265-271.
Stireman, J.O. III, J.E. O’Hara, D.M. Wood, D.M. 2006. Behavior, ecology
and evolution of tachinid parasitoids. Ann. Rev. Entomol. 51: 525-555.
Stireman, J.O. III, M.S. Singer. 2003. What determines host range in
parasitoids? An analysis of a tachinid parasitoid community. Oecologia
135: 629-638.
Karen Oberhauser is an Associate Professor in the Dept. of Fisheries, Wildlife and Conservation Biology at the University of Minnesota. She and her
students conduct research on several aspects of monarch butterfly ecology,
including reproductive ecology, host-parasite interactions, factors affecting
the distribution and abundance of immature monarch stages, risks posed
by global climate change and pest control practices to monarch butterflies.
She and her student Michelle Prysby started the Monarch Larva Monitoring
Project in 1996.
Instant symposiuM
The Lost Ladybug Project:
Citizen Spotting Surpasses Scientist’s Surveys
John Losey, Leslie Allee, and Rebecca Smyth
C
occinellids, known as ladybugs, ladybeetles, or ladybird beetles,
are among the most common and easily recognizable invertebrate components of almost every terrestrial ecosystem in
the U.S. and Canada (Gordon 1985). Species in this family are so
ubiquitous and yet so sensitive to environmental conditions that they
have been proposed as indicator species (Iperti 1999). In addition to
their ubiquity, the bright coloration and gentle nature of this group
make them a favorite wild creature of adults and youth alike. Like
honeybees, ladybugs are revered for their industriousness and their
important ecological role as well as their beauty.
This respect is well deserved, as ladybugs contribute to the control
of many pest insect species (reviewed in Hodek and Honěk 1996).
Given their potential to control pest species, many programs have
tried to supplement extant populations or introduce new species.
22
Ladybugs have been the subject of many scientific studies, and from
these studies we know that ladybug species vary greatly in their
ability to suppress pest populations (reviewed in Hodek and Honěk
1996) and their response to changing environmental conditions
(Iperti 1999; Bazzocchi et al. 2004). Thus, long-term regional shifts
in species composition may have important implications for the functioning of this complex and its response to environmental changes.
Over the past twenty years, several native ladybug species that were
once very common have become extremely rare (Harmon et al. 2006).
During this same time, several species of ladybugs from other places
have greatly increased both their numbers and range (Harmon et al.
2006). This has occurred very quickly, and we don’t know how this shift
happened, what impact it will have (e.g., whether the exotic species
will be able to control pests as well as our familiar native ones have),
American Entomologist  • Spring 2012