Life History and Potential Hosts of Zapatella davisae (Hymenoptera: Cynipidae), a Recent Invader on Black Oak
in the Northeastern United States
Monica Davis, Joseph Elkinton, and Russell Norton
Northeastern Naturalist, Volume 24, Issue 4 (2017): 526–535
Full-text pdf (Accessible only to subscribers. To subscribe click here.)
Access Journal Content
Open access browsing of table of contents and abstract pages. Full text pdfs available for download for subscribers.
Current Issue: Vol. 30 (3)
Check out NENA's latest Monograph:
Monograph 22
Northeastern Naturalist
526
M. Davis, J. Elkinton, and R. Norton
22001177 NORTHEASTERN NATURALIST 2V4(o4l). :2542,6 N–5o3. 54
Life History and Potential Hosts of Zapatella davisae
(Hymenoptera: Cynipidae), a Recent Invader on Black Oak
in the Northeastern United States
Monica Davis1,*, Joseph Elkinton1, and Russell Norton2
Abstract - Quercus velutina (Black Oak) is a dominant deciduous tree in Cape Cod, Martha’s
Vineyard, and Nantucket, MA. In recent years, Black Oak trees in these regions have
experienced severe canopy loss due to the infestation of a stem-gall wasp, Zapatella davisae.
In addition to infestations first documented in the Cape Cod region in 2012, Zapatella
davisae has been present in Long Island, NY, since the 1990s. We investigated the life cycle
of Z. davisae, specifically emergence patterns and timing of development. We evaluated differences
in the severity of the infestations in Long Island and Cape Cod. We also identified
towns in Cape Cod that contained Z. davisae infestations to better estimate the geographic
extent of the infestation in the region. We found that Zapatella davisae completes 1 generation
per year and emerges throughout the month of May. The severity of the infestation
was the greatest in Cape Cod, an indication that something is controlling the population in
Long Island. We concluded that Z. davisae is widespread and present in all towns in Cape
Cod, Nantucket, and Martha’s Vineyard. Our research will lay the foundation for future biological
control efforts and will help arborists and landowners make management decisions
regarding Z. davisae in the Cape Cod region and Long Island.
Introduction
Oaks are a major component of New England forests, therefore oak pests can
have lasting economic and ecological impacts on the region. In particular, a stem
gall wasp, Zapatella davisae Buffington and Melika (Hymenoptera: Cynipidae),
has caused extensive mortality and canopy damage to Quercus velutina Lam.
(Black Oak) in Cape Cod, Nantucket, and Martha’s Vineyard, MA (Buffington et
al. 2016). Cape Cod is the largest protected coastal area of oak–pine forest or sandplain
vegetation in New England (Eberhardt et al. 2003). It is composed of sandy
soil that is often nutrient poor and does not retain water; thus, trees that can adapt to
dry, low-nutrient conditions are the most successful competitors (Neil et al. 2007).
Drought-resistant tree species, such as Pinus rigida Mill (Pitch Pine.), Black Oak,
and Quercus coccinea Muenchh. (Scarlet Oak) make up most of the trees in this
forest (Eberhardt et al. 2003). A decline in Black Oak tree canopy cover is of high
conservation concern in the Cape Cod region.
Zapatella davisae was discovered on Martha’s Vineyard in 2012, but infestations
can be tracked back to ca. 2008 based on the inferred ages of damaged twigs
and branches (Buffington et al. 2016). Zapatella davisae creates woody stem galls
1University of Massachusetts Amherst, 160 Holdsworth Way, Amherst, MA 01002.
2Cape Cod Extension, 3195 Main Street, Barnstable, MA 02563. *Corresponding author -
mjdavis@eco.umass.edu.
Manuscript Editor: Daniel Pavuk
Northeastern Naturalist Vol. 24, No. 4
M. Davis, J. Elkinton, and R. Norton
2017
527
underneath the bark and causes extensive node swelling and twig disfiguration
(Fig. 1; Buffington et al. 2016). Other symptoms include flagging, leaf clumping,
canopy dieback, and tree mortality (Fig. 2; Pike et al. 2001). Although the damage
caused by Z. davisae has been documented in individual trees, its life cycle, severity
of damage, and host specificity have remained unknown (Buffington et al. 2016).
Part of our research parallels a previous study of an oak-gall wasp (previously
misidentified as Bassettia ceropteroides Bassett) that caused damage and mortality
to Black Oak on Long Island in 1990 (Melika and Abrahamson 2007). Over the past
Figure 1. Female Zapatella
davisae, collected in
Dennis, MA (41.7370°N,
70.1933°W).
Figure 2. Damage to Quercus velutina (Black Oak), by Zapatella davisae. (a) Twiggall
damage including swollen nodes and stems (b) Z. davisae cavities on a Black Oak
branch, (c) exit holes from Z. davisae adults on Black Oak, and (d) a heavily damaged
Black Oak tree.
Northeastern Naturalist
528
M. Davis, J. Elkinton, and R. Norton
2017 Vol. 24, No. 4
5 years, there has been much speculation as to whether B. ceropteroides is the same
species that is causing extensive tree mortality in Cape Cod, Martha’s Vineyard, and
Rhode Island. In 2016, molecular analyses confirmed that the gall wasp on Long
Island is the same species that is on Cape Cod (Buffington et al. 2016), and not long
after, taxonomists determined that the gall wasp is a new species, Zapatella davisae
(Buffington et al. 2016). Differences between the 2 populations, specifically host
trees and the severity of the infestation have not been previously evaluated.
Zapatella davisae is a member of the Cynipini, a host-specific tribe that contains
over 87% of all gall makers on oaks (Abrahamson 1998, Stone et al. 2008).
Life-cycle descriptions are available for only 85 of 900 species in the Cynipini tribe
worldwide (Pujade-Villar et al. 1999). The life cycle of Z. davisae is still unknown;
however, the biology of other species of Zapatella may help identify potential lifecycle
patterns. All Cynipini, also known as oak-gall wasps, reproduce through either
cyclic or obligate parthenogenesis (Stone et al. 2008). Cyclic parthenogenesis in
Cynipini consists of the strict alternation between 1 parthenogenetic generation and
1 sexual generation (Stone et al. 2008). The alternating generations may occur in the
same year or in alternating years and may attack different hosts or different tissues
of the same host (Hood and Ott 2001, Stone et al. 2002). Obligate parthenogenesis is
also common in Cynipini, having evolved many times from cyclic parthenogenesis
by deletion of the sexual generation (Herbert 1981, Rispe and Pierre 1998).
Most Zapatella species exhibit obligate parthenogenesis; however, they have
various hosts, gall-tissue types, and generation times. For example, Zapatella
nievesaldreyi Melika and Pujade-Villar induces stem galls on Quercus humboldtii
Bonpl. (Andean Oak) in Colombia, whereas Zapatella oblata Weld creates
bud galls on both Scarlet Oak and Quercus falcata Michx (Southern Red Oak) in
Virginia (Pujade-Villar et al. 2012). Preliminary microsatellite data (J. Andersen,
University of California Berkley, Berkley, CA, unpubl. data) suggest that sampled
populations of Z. davisae are obligately parthenogenetic, but it is unclear whether
cyclic parthenogenesis also occurs.
An understanding of the life cycle, severity of the infestation, and potential
hosts of Z. davisae will aid in determining future management efforts and help
answer ecological questions regarding Z. davisae community and population dynamics.
Our first objective was to describe the life cycle of Z. davisae, specifically
its emergence patterns and the phenology of its developmental stages. Our second
objective was to compare levels of infestation between Cape Cod and Long Island,
and identify any additional host trees in each region. Our final objective was to
document the distribution of Z. davisae in Cape Cod. Our research will inform the
implementation of different management strategies, as well as identify the geographical
distribution and potential hosts of Z. davisae.
Field-site Description
We conducted all field collections and surveys in coastal sand-plain vegetation
communities in New England and Long Island, NY. We completed infestation
surveys in Cape Cod, Nantucket, and Martha’s Vineyard, MA, as well as Long
Northeastern Naturalist Vol. 24, No. 4
M. Davis, J. Elkinton, and R. Norton
2017
529
Island, NY, and coastal Rhode Island. All locations were in close proximity to the
coast and contained oak–pine forest vegetation. We undertook the life-cycle study
at 2 sites: 1 in Dennis, MA (41°44'12.33'' N, 70°11'38.78''W) and the other in Riverhead,
NY (40°57'44.26''N, 72°42' 59.57''W).
Methods
Life cycle
To determine emergence patterns of Z. davisae, we captured adult gall wasps as
they emerged from stem galls in Cape Cod, MA. We covered new and last year’s
growth on 100 branches of 20 infested trees with 11.4 cm x 17.7 cm organza bags.
We made visual inspections of the bags each month from November 2013 to March
2014, and then weekly during April and May 2014. At each check, we scored every
bag for the presence or absence of Z. davisae. We completed the same schedule
of bag deployment and visual checks the following year, from November 2014 to
May 2015. To determine date of emergence, we recorded dates when live gall wasps
were found and calculated a range based on the first and last re cord.
We collected branch samples biweekly from Dennis, MA, and Riverhead, NY, to
document the stages of development of the stem-gall generation. Every other week,
we haphazardly collected and stored in separate 3.79-L (1-gallon) plastic bags 5
branches from the crown of 10 trees at 1 of the 2 sites. We performed dissections of
the galls on new and last year’s growth under a dissecting microscope (Wild M5A,
6x–50x), and scored each sample for the presence or absence of each life stage of
Z. davisae. We did not conduct statistical analyses of these data because we used
the binomial data only to identify the timing of certain life stages.
Tree infestation survey
During the spring and summer of 2016, we completed field surveys on Long
Island and Cape Cod. We randomly chose GPS coordinates of 7 sites per region
that contained Pitch Pine and oak forest vegetation on a GIS topographical map;
all locations were at least 10 km from any other site. We checked each site, and if
Black Oak trees were not present, we drove no more than an additional 3 km in
search of trees. If we were unable to find Black Oak, we randomly chose a new
site in the same manner. At each of the 7 sites in both regions, we scored 20 Black
Oak trees for the presence or absence of gall-wasp infestation. At each site, we
identified to species each oak tree that was not a Black Oak and was scored for
the presence or absence of gall-wasp infestation. We scored level of infestation
on field observations. We defined low-infested trees as those with small galls that
were difficult to find, moderately infested trees had obvious galls and noticeable
canopy damage, and heavily infested trees had >80% of branches galled and severe
canopy damage. We used RStudio Version 0.99.491 (R Core Team 2015) to
run a chi-squared test comparing the number of trees at each infestation level between
both regions, and to perform a 2-sample test for equality of proportions and
chi-square to compute the proportion of trees infested in each region.
Northeastern Naturalist
530
M. Davis, J. Elkinton, and R. Norton
2017 Vol. 24, No. 4
Estimation of gall-wasp distribution
We surveyed by car and on foot towns in Rhode Island, Cape Cod, Martha’s
Vineyard, and Nantucket to identify places where Z. davisae was present in New
England. We and extension personnel completed visual surveys in each region. The
main focus of this project was Cape Cod, Martha’s Vineyard, and Nantucket; however,
we also documented infestations reported in Rhode Island. We surveyed all
towns in Cape Cod, Martha’s Vineyard, and Nantucket, MA. In Rhode Island, we
searched only coastal areas for Z. davisae with local extension personnel. Zapatella
davisae was scored as being present in a town if observers detected Z. davisae damage
on at least 5 trees. We overlaid a GIS layer from the Massachusetts Department
of Conservation and Recreation to compare defoliation levels with town-level infestation
detection. We created a map in QGIS Version 2.180 to identify the current
extent of the Z. davisae infestation.
Results
Life cycle
We detected no gall wasp emergence in the fall of 2013 and 2014 of the bag
experiment, confirming that Z. davisae does not have an autumnal generation. In
the spring of 2014, Z. davisae adults emerged 7–25 May on Cape Cod. We observed
the same pattern in 2015 and concluded that Z. davisae emerges between the 1st and
3rd week of May depending on the year.
The life cycle of 1 generation of Z. davisae from August to May is illustrated
diagrammatically in Figure 3. The Z. davisae life stages we recognized included
early and late larval stages, pupae, and fully formed adults. We first detected gall
cavities in July, and the early larval stage was present by mid-August, with the
late larval stage present in early September. We did not determine the number of
Figure 3. Timing and
stages of development
for the twig-gall
generation of Zapatella
davisae.
Northeastern Naturalist Vol. 24, No. 4
M. Davis, J. Elkinton, and R. Norton
2017
531
larval instars. Pupation occurred in mid-September, when both larval stages were
still present. In early October, we detected pharate adults. Mature adults were
present in early spring of the following year and they emerged in May. Zapatella
davisae overwintered in several life stages, and individuals became adults by May
prior to emergence.
Tree-infestation surveys
There was a significant difference in the level of gall-wasp infestation on Long
Island versus Cape Cod (χ 2 = 30.6; df = 3; P < 0.0001; Fig. 4). Long Island had significantly
more trees with low-level infestations than trees with medium or heavy
infestations. Cape Cod showed the opposite trend, with more heavy infestations,
followed by medium and then low infestations. There was a site effect on both Cape
Cod and Long Island, confirming that infestation levels varied across both regions
(Cape Cod: χ 2 = 95.633; df = 18; P < 0.0001; Long Island: χ 2 = 53.438, df = 18,
P < 0.0001). No other oak species besides Black Oak was infested by Z. davisae
(Table 1). Most Black Oaks in both regions harbored some infestation, and the
Table 1. Number of trees surveyed for each oak species at sites on Cape Cod and Long Island and
the proportion of trees of each species that were infested with Zapatella davisae (all zero except for
Black Oak)
Number trees surveyed (proportion infested)
Oak species Cape Cod Long Island
White 24 (0.00) 0 (0.00)
Red 9 (0.00) 4 (0.00)
Scarlet 11 (0.00) 1 (0.00)
Chestnut 0 (0.00) 2 (0.00)
Pin 0 (0.00) 2 (0.00)
English 4 (0.00) 0 (0.00)
Black 120 (0.89 ± 0.027 SE) 120 (0.79 ± 0.037 SE)
Figure 4. Average
proportion
of trees at each
gal l -wasp infestation
level
(low, medium,
and high) across
all sites on Long
Island and Cape
Cod.
Northeastern Naturalist
532
M. Davis, J. Elkinton, and R. Norton
2017 Vol. 24, No. 4
Figure 5. Map of towns in New England with known Zapatella davisae infestations documented
by ground surveys. Includes Z. davisae defoliation data from DCR mapping flyovers
in 2015 and 2016.
proportion of trees infested in Cape Cod versus Long Island was not different
(Table 1) (χ 2 = 3.745; df = 1; P = 0.052).
Estimation of gall wasp distribution
All towns on Cape Cod contained a Z. davisae infestation (Fig. 5). Zapatella davisae
was present in all towns on Nantucket and Martha’s Vineyard. In Rhode Island,
documented infestations were in primarily coastal areas of oak–pine forest, where
Black Oak was the dominant deciduous tree. Zapatella davisae defoliation levels
reported in maps by the Massachusetts Department of Conservation and Recreation
(DCR) Forest Health Program in 2015 and 2016 were consistent with our survey results
(MA DCR 2016); however, Z. davisae was found in 12 additional towns where
the overhead defoliation data of the DCR survey did not detect Z. davisae.
Discussion
We found that Z. davisae completes one stem-gall generation per year, and
emerges in May. This life cycle is congruent with the biology of several other Zapatella
species (Pujade-Villar et al. 2012). Identifying the life cycle of Z. davisae
will allow managers to determine the appropriate timing for biological-control
release or pesticide application. Z. davisae only has 1 life cycle per year; thus, it
should be easier to manage than other gall wasp pests with multiple generations
(Bhandari and Zhiqiang 2016). We have conducted a follow-up study to evaluate
the efficacy of systemic insecticides as control agents of Z. davisae and intend to
Northeastern Naturalist Vol. 24, No. 4
M. Davis, J. Elkinton, and R. Norton
2017
533
give application date recommendations based on Z. davisae’s life cycle (M. Davis
and J. Elkinton, unpubl. data).
Zapatella davisae was first noted on Martha’s Vineyard in 2008 and has continued
to be detected in significant portions of the oak–pine forest in coastal New
England. We observed Z. davisae only attacking Black Oak in the field; thus, its
potential for range expansion throughout New England may be limited by the distribution
of Black Oak. In New England, Black Oak occurs widely, but it is only
a dominant deciduous tree in coastal oak–pine forests. Our results indicate that
Z. davisae may not have the capacity to establish inland, but will continue to be
a coastal pest in areas with sand-plain vegetation. Thus far, we have encountered
Z. davisae only in this forest type.
Native species whose ranges are expanding have the capacity to alter native
plant communities and population dynamics (Prior and Hellmann 2013, Schonrogge
et al. 1995). Some native insect herbivores have little impact on their host plant
due to the suppression of population densities by natural enemies (i.e., top-down
control; Keane and Crawley 2002, Strong et al. 1984). Other species may experience
natural-enemy release during a lag period after initial expansion, which can
lead to population outbreaks and extensive plant damage (Prior and Hellman 2013).
Our results imply that temporal and spatial differences between Long Island and
Cape Cod populations have influenced the population dynamics of Z. davisae. It is
evident that Z. davisae causes significantly more damage on Cape Cod than Long
Island. Based on the enemy-release hypothesis, these new populations on Cape Cod
may be causing more damage, because they are released from their natural enemies,
which would otherwise keep them in check. As for next steps, we have identified
parasitoids in both regions and plan to utilize population-ecology methods to evaluate
their effect on Z. davisae’s population dynamics.
Extensive Black Oak mortality in coastal New England has caused significant
ecological and economic impacts, including the cost of removing and replacing
dead trees. We identified preliminary information about Z. davisae’s biology, specifically
its life cycle, symptoms, and distribution. This information provides a
strong foundation for integrated pest management practices and helps describe a
pest that was once unknown to science. In addition, our study revealed the need to
evaluate factors that influence Z. davisae populations on Long Island and Cape Cod,
including pesticide control and natural-enemy regulation.
Acknowledgments
We thank H. Broadley, T. Murphy and J. Boettner, from the University of Massachusetts-
Amherst, for manuscript review and feedback. We are grateful to D. Gilrein, from the
Cornell Horticultural station, and H. Faulbert, from the University of Rhode Island, for
help finding field sites. We appreciate undergraduate students E. Mooshain, C. Camp, G.
Hepsler, and K. Donahue for field collection and processing help. We thank Arborjet Inc.,
the Woodbourne Arboretum, and the University of Massachusetts-Amherst Department of
Environmental Conservation for funding support.
Northeastern Naturalist
534
M. Davis, J. Elkinton, and R. Norton
2017 Vol. 24, No. 4
Literature Cited
Abrahamson, W.G., G. Melika, R. Scrafford, and G. Csoka. 1998. Gall-inducing insects
provide insights into plant systematic relationships. American Journal of Botany
85:1159–1165.
Bhandari, B.P., and C. Zhiqiang. 2016. Trunk injection of systemic insecticides to control
stem- and leaf-gall wasps, Josephiella species (Hymenoptera: Agaonidae), on Chinese
Banyan (Rosales: Moraceae) in Hawaii. Florida Entomology 99:172 –177.
Buffington, M., G. Melika, M.J. Davis, and J.E. Elkinton. 2016. The description of Zapatella
davisae, new species, (Hymenoptera: Cynipidae) a pest gall-wasp of Black Oak
(Quercus velutina) in New England, USA. Proceedings of the Entomological Society of
Washington 118(1):14–26.
Eberhardt, R.W., D.R. Foster, G. Motzkin, and B. Hall. 2003. Conservation of changing
landscapes: Vegetation and land-use history of Cape Cod national seashore. Ecology
13:68–84.
Herbert, P. 1981. Obligate asexuality in Daphnia. American Naturalist 117:784–789.
Hood, G.R., and J.R. Ott. 2011. Generational shape shifting: Changes in egg shape and
size between sexual and asexual generations of a cyclically parthenogenetic gall former.
Entomologia Experimentalis et Applicata 141:88–96.
Keane, R.M., and M.J. Crawley. 2002. Exotic plant invasions and the enemy hypothesis.
Trends in Ecology and Evolution 17:164–170.
Massachusetts Department of Conservation and Recreation (MA DCR). 2016. 2015 and
2016 Aerial Survey. Forest Health Program, Worcester, MA.
Melika, G., and W. Abrahamson. 2007. Review of the Nearctic gallwasp species of the
genus Bassettia Ashmead, 1887, with description of new species (Hymenoptera: Cynipidae:
Cynipini). Acta zoologica Academiae Scientiarum Hungaricae. 53(2):131–148.
Neil, C., B. Von Hollen, K. Kleese, K.D. Ivy, A.R. Collins, C. Treat, and M. Dean. 2007.
Historical influences on the vegetation and soils of the Martha’s Vineyard, Massachusetts
coastal sand plain: Implications for conservation and restoration. Biological Conservation
136:17–32.
Pike, C., D. Robison, and L. Abrahamson. 2001. Black Oak decline on New York’s Long
Island 1990–1996. USDA Forest Service, Newtown Square, PA.
Prior, K.M., and J.J. Hellmann. 2013. Does enemy loss cause release? A biogeographical
comparison of parasitoid effects on an introduced insect. Ecology 94:1015–1024.
Pujade-Villar, J., D. Bellido, G. Segu, and G. Melika. 1999. Current state of heterogony
in Cynipidae (Hymenoptera, Cynipoidea). Sessió Conjunta d'Entomolo gia 11:87–107.
Pujade-Villar, J., P. Hanson, C.A. Medina, M. Torres, and G. Melika. 2012. A new genus
of oak-gall wasps, Zapatella Pujade-Villar & Melika, gen. n., with a description of
two new species from the Neotropics (Hymenoptera, Cynipidae, Cynipini). ZooKeys
210:75–104.
R Core Team. 2015. R Studio–Integrated Development for R. RStudio, Inc., Boston, MA.
Available online at www.rstudio.com. Accessed June 2014.
Rispe, C., and J.S. Pierre. 1998. Coexistence between cyclical parthenogens, obligate
parthenogens, and intermediates in a fluctuating environment. Journal of Theoretical
Biology 95(1):97–110.
Schonrogge, K., G.N. Stone, and M.J. Crawley. 1995. Spatial and temporal variation in
guild structure: Parasitoids and inquilines of Andricus quercuscalicis in its native and
alien ranges. Oikos 72:51–60.
Northeastern Naturalist Vol. 24, No. 4
M. Davis, J. Elkinton, and R. Norton
2017
535
Stone, G.N., K. Schonrogge, R.J. Atkinson, D. Bellido, and J. Pujade-Villar. 2002. The
population biology of oak-gall wasps (Hymenoptera: Cynipidae). Annual Review of
Entomology 46:633–668.
Stone, G.N., R.J. Atkinson, A. Rokas, J.L. Aldrey, G. Melika, Z. Acs, G. Csoka, A. Hayward,
R. Bailey, C. Buckee, and G.A.T. McVean. 2008. Evidence for widespread cryptic
sexual generations in apparently purely asexual Andricus gall wasps. Molecular Ecology
17:652–665.
Strong, D.R., J.H. Lawton, and R. Southwood. 1984. Insects on plants: Community Patterns
and Mechanisms. Blackwell Scientific, Oxford, UK. 313 pp.