BioControl (2014) 59:659–669 DOI 10.1007/s10526-014-9604-9
Patterns of parasitoid host utilization and development across a range of temperatures: implications for biological control of an invasive forest pest Jian J. Duan • David E. Jennings • Dontay C. Williams • Kristi M. Larson
Received: 30 April 2014 / Accepted: 7 July 2014 / Published online: 23 July 2014 Ó US Government 2014
Abstract Although climate change frequently has been linked to observed shifts in the distributions or phenologies of species, little is known about the potential effects of varying temperatures on parasitoids and their relationships with hosts. Using the egg parasitoid Oobius agrili (Hymenoptera: Encyrtidae) we examined host utilization patterns of this species across a range of temperatures (20–35 °C) to explore how changing climate could affect the interaction with its host—the emerald ash borer (EAB) (Coleoptera: Buprestidae), a serious invasive forest pest that has killed tens of millions of ash (Fraxinus spp.) trees in North America. Results from our study showed that the window of host susceptibility to O. agrili parasitism declined significantly from 14.8 to 2.6 days in an inverse second-order relationship with increasing exposure temperatures from
Handling Editor: Stefano Colazza. J. J. Duan (&) D. C. Williams Beneficial Insects Introduction Research Unit, Agricultural Research Service, United States Department of Agriculture, 501 South Chapel Street, Newark, DE 19713, USA e-mail:
[email protected]
20 to 35 °C. In contrast, parasitoid host attack rate changed in a bell-shaped second-order relationship— i.e., increased with temperatures from 20 to 25 °C, but decreased at about the same rate when temperatures increased from 30 to 35 °C. This range of temperatures also significantly affected the development and mortality of immature parasitoids with 35 °C resulting in 100 % mortality. There was little mortality (0–4.5 %) and no significant differences in the percentage (20.9–34.9 %) of immature O. agrili that entered diapause (as mature larvae) at 20, 25, and 30 °C. However, there were significant differences in the time event of adult wasp emergence within this temperature range. The median time for 50 % of immature O. agrili emerging as adults at 20, 25, and 30 °C were 38, 18, and 17 days after parental wasp oviposition, respectively. Together these findings indicate that the non-linear and unequal temperature effects on these host utilization parameters are likely to result in differential host parasitism rates, and thus could reduce the efficacy of this parasitoid in suppressing host populations due to climate change (global warming and extreme heat). Keywords Egg parasitoid Forest pest Climatic change Invasive Agrilus planipennis
D. E. Jennings Department of Entomology, University of Maryland, College Park, MD 20742, USA
Introduction
K. M. Larson Department of Entomology and Wildlife Ecology, University of Delaware, Newark, DE 19713, USA
Climate change frequently has been linked to observed shifts in distributions or phenologies of species
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(Parmesan 2006, 2007; Hance et al. 2007). Such shifts pose a significant threat to global biodiversity (Thomas et al. 2004; Thuiller et al. 2005; Deutsch et al. 2008), for instance by causing a loss of suitable habitat for range-restricted species, or phenological mismatches between predators and prey. In addition, climate change can also affect the outbreak of insect pests either via direct impacts on their range expansion and temperature-driven, developmental rates or via indirect impacts on their abundance from trophic interactions with host plants (bottom–up) or natural enemies (top–down) (Berggren et al. 2009; Klapwijk et al. 2012). From a pest management perspective, the potential impact of climate change on trophic interactions between insects and their natural enemies (predators or parasitoids) may lead to less effective control of the pest populations from top–down effects (Klapwijk et al. 2012). Consequently, furthering our understanding of how invasive pests and their natural enemies will respond to climate change (e.g., global warming and extreme heat) should enable us to better mitigate any future adverse effects on global biodiversity and invasive pest management. Invasive forest insect pests are a major concern worldwide because they can be easily transported through live plant materials and wooden shipping crates via increased global trade (Liebhold et al. 1995; Mattson et al. 2007; Aukema et al. 2010; Yang et al. 2014). Climate change has already been implicated as being responsible for increased damage and range expansion of several invasive forest insects (Moraal and Akkerhuis 2011; Ju et al. 2013), and in the United States alone over 450 species of invasive forest insects have become established (Aukema et al. 2011). The scale of natural forests can be prohibitive (both environmentally and financially) for the widespread use of chemical treatments to control invasive insects, and therefore the introduction of biocontrol agents (i.e., natural enemies) from the pest’s native range is sometimes a preferable management option. However, very little is known about the potential effects of climate change on parasitoids and their interactions with hosts (Klapwijk et al. 2010; Jeffs and Lewis 2013). Emerald ash borer (EAB), Agrilus planipennis (Coleoptera: Buprestidae), is a devastating invasive pest of ash trees (Fraxinus spp.) in North America that is thought to have been inadvertently introduced to the continent from northeast Asia in the 1990s. In
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sufficient numbers the galleries created by EAB larvae effectively girdle and kill their host trees, and thus far this beetle has killed tens of millions of ash trees causing extensive ecological and economic losses in the United States and Canada (Cappaert et al. 2005; Kovacs et al. 2010; Herms and McCullough 2014). EAB has also caused significant damage to North American species of ash planted in China and Russia (Straw et al. 2013), making it an insect of increasingly global importance. Natural enemies native to China have been introduced into North America for EAB biocontrol, including two larval parasitoids and one egg parasitoid, Oobius agrili (Hymenoptera: Encyrtidae). Oobius agrili is a small (*1 mm in size), solitary idiobiont egg parasitoid, first collected in northeast China (Jilin Province) and described by Zhang et al. (2005). Female O. agrili produce an average of 60 eggs (per wasp) in a lifetime through thelytokous parthenogenesis in the laboratory (JJD, unpublished data), and can have multiple generations per year in its native range in the field (Liu et al. 2007). In China, O. agrili can be responsible for 28–60 % of EAB egg mortality (Liu et al. 2007), and is potentially more beneficial for ash conservation than larval parasitoids because reducing egg densities should limit the damage that EAB larvae cause to ash trees. However, O. agrili has only been collected from EAB in northeast China (Heilongjiang, Liaoning and Jilin Provinces), and not further south such as in Hebei Province (Liu et al. 2007; JJD unpublished data; personal communication with Dr. Xiao Yi Wang, Chinese Academy of Forest Science), where abundant populations of EAB also occur (Wei et al. 2004, 2007). To date, there have been no studies on critical factors such as climatic conditions that limit the distribution of O. agrili in its native range. It is known that O. agrili successfully overwinters via both facultative and obligatory diapause as mature larvae in northeastern China (JJD, unpublished data), where the average winter temperature can be as low as -20 °C with -38 °C as the extreme (National Meteorological Information Center of China 2014). Winter temperature is generally much higher in southern China in comparison to the north, and thus it appears as though winter temperature is not likely to limit the range distribution of O. agrili. Alternatively, because EAB oviposition occurs in the summer months (from June to August), the temperature range in those months (monthly average ranging from 16 to 31 °C
Biological control of an invasive forest pest
with 41 °C as the extreme) may have profound impacts on the abundance and distribution limit of O. agrili in its native range. Oobius agrili has been released for biocontrol of EAB in the United States since 2007 (Duan et al. 2011). There is some evidence that O. agrili has started to establish in North America, although parasitism rates are not yet comparable to those in the native range (Duan et al. 2012a). While the distribution of EAB in North America is predicted to expand northwards under future climate change scenarios (Liang and Fei 2014), little consideration has yet been given to how these changes will affect the interaction of this pest with its natural enemies such as O. agrili (but see Gould et al. 2011). This could have important implications for future EAB population dynamics and biocontrol efforts. For example, phenological mismatch could occur between EAB and O. agrili, or the range expansion of EAB could outpace that of the egg parasitoids (Menendez et al. 2008). Given the paucity of information on O. agrili biology and ecology, here we examine host utilization of this species across a range of temperatures to investigate the potential effects of climate change on its interaction with EAB. The temperature range we selected for the study was from 20 to 35 °C, as these temperatures permit the survival and development of EAB eggs in both the laboratory and field (Wei et al. 2004, 2007; Duan et al. 2013). We tested how different treatment temperatures affected: (1) the window of susceptibility for EAB eggs to O. agrili parasitism, (2) the host attack rate of O. agrili, and (3) the development, diapause, and mortality of immature O. agrili. Because of the effects of increased temperature on metabolic rate of insects (Gilbert and Raworth 1996), we predicted that temperature would reduce the window of susceptibility of EAB eggs for parasitoids and the development time, while increasing the attack rate of O. agrili.
Materials and methods Parasitoids Oobius agrili used in this study were F10–30 progeny of a founder colony originally collected from northeast China (Liaoning and Jilin Provinces) between 2008
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and 2010. This colony had since been reared with natural host EAB eggs. Throughout the investigation, we utilized only naı¨ve wasps (i.e., those with no previous exposure to host eggs). Before experiments, adult parasitoids were housed in ventilated clear 12 ml plastic tubes (each 12 cm long 9 1 cm in diameter, Tri-State Plastics, Latonia, KY, USA) and maintained in environmental chambers (Percival Scientific, Perry, Iowa, USA) at 25 (±1) °C, with 65 ± 10 % RH and 16:8 (L:D) hour photoperiod. A food source was offered to the parasitoids by streaking clover honey on the inside wall of the tube. Host eggs All host eggs originated from adult EAB, which were collected from infested green ash (F. pennsylvanica) trees in Maryland and reared with bouquets of fresh green (F. pennsylvanica) or tropical (F. uhdei) ash leaves according to procedures described in Duan et al. (2013). Briefly, the beetle rearing procedure involved in hosting gravid females in a 1 l ventilated plastic (oviposition) cups at a density of approximately five females and two–three males per cup, and provided with fresh host plant leaves every two or three days. To obtain EAB eggs, the mouth of the oviposition cup was covered with nylon screen (mesh size *1 mm2) and then with a sheet of coffee filter paper (8.25 cm base, HomeLifeTM, Eden Prairie, MN, USA) on the top to serve as a suitable oviposition site (Duan et al. 2012b). Gravid EAB females were attracted to lay eggs on the screen covered substrates such as coffee filter paper (Yang et al. 2012). EAB eggs laid on the coffee filter paper were then used in different experiments with temperature treatments. Effect of temperature on windows of host egg susceptibility to parasitism Coffee filter papers with freshly laid host eggs (within 24 h) were cut into small individual pieces (*8–10 cm long 9 3–4 mm wide), each with 5–10 eggs, and placed inside the 15 ml ventilated plastic tubes secured with loosely-screwed caps. Plastic tubes containing freshly laid host eggs (10–12 eggs per vial) were placed inside ventilated Crisper Boxes and then housed in growth chambers (ARB-366, Percival Scientific Inc., Perry, Iowa, USA) set with constant RH (60 ± 5 %) and photoperiod (16:8 h L:D) but
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After 24 h of exposure to the host eggs, wasps were removed from the test tubes. Immediately following the removal of test wasps, exposed host eggs inside the test tubes were incubated in the normal rearing chamber for approximately 4–6 weeks and then scored for parasitism based on the adult emergence exit holes, presence of diapaused (live) parasitoid larvae, and/or cadavers (if the parasitoids were dead). A total of 25 wasps (each with ten host eggs) were tested at each temperature treatment.
different temperature treatments (constant 20, 25, 30 and 35 °C, respectively) for host egg aging. For each temperature treatment, four to five age groups of host eggs (each with 10–12 eggs) were created with this procedure at different time intervals. The time interval for aging host eggs varied from every three or four days for the lower temperature (20 and 25 °C) treatments to every one or two days for the higher temperature (30 and 35 °C) treatments. However, all host eggs prepared for aging at different time intervals for each temperature treatment had to reach their targeted ages at the same time for exposure to parasitoids. A control group (consisting of freshly laid eggs) was included for exposure to parasitoids for each temperature treatment. Tests of different age groups with parasitoids for each temperature were replicated five times. For testing, five gravid O. agrili wasps (5–7 days old after emergence) were introduced with a small camel-hair brush into each plastic vial containing host eggs (10–12 per vial). Vials containing host eggs and adult parasitoids were then placed inside a large container (Crisper Box or 500 ml-cups) hosted in a growth chamber set with normal rearing conditions (25 °C, 60 ± 5 % RH, and 16:8 h L:D photoperiod). Parasitoids were removed from all the test vials after 24 h of exposure to host eggs and exposed host eggs were incubated under normal rearing conditions for 4–6 weeks prior to determination of parasitism. By then, parasitism by O. agrili was easily scored based on the number of emerged adult wasps, and dissection of darkened (parasitized) eggs that contained either live (diapaused) mature larvae or dead parasitoid cadavers.
The developmental rate and time to adult, diapause and mortality of immature O. agrili were evaluated across the same temperature (20, 25, 30 and 35 °C) treatments as described previously. Host eggs freshly laid on pieces of filter paper were first exposed to gravid O. agrili in the test tubes at a host to parasitoid ratio of 2:1 (ten host eggs with five wasps per tube) for 24 h under normal rearing conditions. After the 24 h exposure period and removal of test wasps from test tubes, exposed host eggs inside test tubes were transferred to the respective temperature treatment chambers, and monitored every day for emergence of adult wasps for a maximum of 56 days. All parasitized eggs that did not emerge from each temperature treatment were then dissected to determine their fate— either entering diapause status (live mature larvae) or being dead (dried-up parasitoid cadavers). A total of five exposure assays (replicates, each consisting of ten host eggs exposed to five wasps) were conducted for each treatment temperature.
Effect of temperature on host attack rates
Data analysis
Host egg attack rates by O. agrili were evaluated with the same temperature (20, 25, 30 and 35 °C) treatments as described previously. Prior to testing, individual wasps were transferred into the test tubes (one wasp per tube) and placed inside test chambers for 24 h acclimation to the test temperature. After the 24 h acclimation to the test temperature, host eggs (freshly laid on one or two pieces of coffee filter paper) were then introduced to the test wasp (ten eggs per wasp) hosted inside the test tubes. Our preliminary trials showed that under normal rearing conditions, O. agrili rarely attack more than ten host eggs per day.
The logistic regression model [P = 1/(1 ? e-(a?bt))] was used to analyze the relationship between the probability (P) of a host egg not being utilized (or parasitized) by O. agrili and its age or time (t) of exposure to each treatment temperature, where a is the constant and b the coefficient of the logistic curve. The host egg age (HT50) and 95 % confidence interval (CI) for 50 % of the eggs not being utilized were then inversely predicted using the fitted logistic regression model for each treatment temperature. The HT50 value predicted from each temperature treatment would also represent the mean window of host egg susceptibility (or
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Effect of temperature on development, diapause, and mortality of immature parasitoids
Biological control of an invasive forest pest
suitability) to O. agrili parasitism. A logistic regression model was also used to analyze the effect of both temperature and host egg age on the probability of host eggs not being parasitized by O. agrili. An inverse second order non-linear model was then used to examine the relationship of HT50 and treatment temperature. The relationship between the mean number of host eggs attacked by each O. agrili during 24 h exposure period was analyzed with a second-order regression model: y = c ? ax ? bx2 where c is the model intercept, x the treatment temperature, a the first-order (linear) coefficient for x, and b the second-order coefficient for x2. To obtain the most parsimonious and best fit model, a stepwise approach was used by fitting the simple linear model and the second-order only model and then compared them with the full model (based on F-statistics for model’s lack-of-fit tests). Data on proportion of wasp emergence, diapause and mortality of immature O. agrili from parasitized host eggs reared at different temperature treatments were analyzed with the same logistic regression procedure as described above. The time-related event of O. agrili adults emerging from different treatment temperatures was analyzed using survival analyses through PROC LIFETEST of SAS 12.1 (SAS Institute 2012). The procedure first estimated the time at 25th, 50th and 75th percentile of hatching events for each temperature treatment based on the survival function computed by the product-limit procedure (also called the Kaplan–Meier method), and then compared the emerging event probability curve between temperature treatments by the log-rank test.
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(host egg age: v2 = 225.01, df = 1, P \ 0.0001; temperature: v2 = 314.92, df = 1, P \ 0.0001). The estimates of host egg ages using logistic models for 25, 50, and 75 % of host eggs not being utilized by O. agrili for each treatment temperature are presented in Table 2. Results showed that as the treatment temperature increased from 20 to 35 °C, host age (HT50) for 50 % of the eggs not being utilized by O. agrili decreased from 14.1 to 2.3 days (Table 2). In contrast, HT50 decreased from 8.3 to 4.3 days when the temperature increased from 25 to 30 °C. There was no overlapping of 95 % confidence intervals for the HT50 estimates among different temperatures indicating significant differences in window of host susceptibility to O. agrili parasitism among the temperature treatments. Non-linear regression analysis showed that the window of host egg susceptibility to O. agrili (as measured with HT50) could be described with a nearly perfect fit of an inverse second-order regression model (Fig. 2). Effects on host attack rate The mean number (±SE) of host eggs parasitized by O. agrili (per wasp in 24 h) increased from 2.9 (±0.6) at 20 °C to the peak of 5.4 (±0.7) at 25 °C, and then decreased from 4.6 (±0.6) at 30 °C to the lowest number of 2.6 (±0.6) at 35 °C. Non-linear regression analysis showed that the mean number of host eggs attacked by O. agrili was significantly predicted by treatment temperature with a second-order regression model (Fig. 3; model’s lack-of-fit test: F = 0.6069, df = 1, 100; P = 0.4378), but not with a simple linear regression model (model’s lack-of-fit test: F = 7.1679, df = 2, 100; P = 0.0012).
Results Effects on window of host susceptibility to parasitism Host utilization (parasitism) rate by O. agrili declined with host egg ages at all temperature treatments (Fig. 1). The coefficient of fitted logistic curve for each treatment temperature (Table 1) indicated that the decline in host utilization rate was much faster with host eggs aged at higher treatment temperatures (30–35 °C) than lower ones (25–20 °C). Logistic regression analysis showed highly significant effects of both host egg ages and associated temperature (20–35 °C) on host egg utilization rate by O. agrili
Effects on parasitoid development, diapause and mortality Approximately 75.5, 79.1, and 60.6 % of immature O. agrili successfully developed to adult wasps (emerging from the parasitized host) at 20, 25, and 30 °C, respectively, but no immature O. agrili did so at 35 °C (Table 3). While approximately 24.5, 20.9, 34.9 % of immature O. agrili entered diapause (as mature larvae) with little (0–4.5 %) mortality at 20, 25, and 30 °C, respectively, all immature O. agrili died before reaching mature larvae or adult wasp at 35 °C. Logistic regression analysis detected significant effects of treatment temperature on the
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Fig. 1 Responses of O. agrili to host eggs exposed to different treatment temperatures for different lengths of time (age) with fitted logistic curves for inverse prediction of the window of host susceptibility (see Table 1). Error bars for observed values correspond to (SE)
Table 1 Logistic regression coefficients for the relationship between the probability of hosts not being utilized (or parasitized) by O. agrili and host egg ages under different temperature regimes Temperature (°C)
Coefficient (growth rate)
Standard error
v2
Df
P [ |v2|
20
0.1909
0.0274
48.36
1
\0.0001
25
0.5023
0.0740
46.09
1
\0.0001
30
0.7948
0.1036
58.83
1
\0.0001
35
0.6501
0.0669
94.32
1
\0.0001
Table 2 Host egg age (HT) and 95 % confidence interval limit (days) for 25, 50 and 75 % of the host eggs becoming not attacked by Oobius agrili under different exposure temperature regimesa Temperature (°C)
N
HT25 (95 % CI) (days)a
HT50 (95 % CI) (days)a
HT75 (95 % CI) (day)a
20
198
8.3 (5.8–10.3)
14.1 (12.2–15.4)
19.8 (17.4–23.7)
25
186
6.1 (4.9–6.9)
8.3 (7.4–9.2)
10.4 (9.5–11.2)
30
196
2.9 (2.2–3.5)
4.3 (3.9–4.9)
5.7 (5.1–6.5)
35
510
0.7 (0.1–1.1)
2.3 (2.0–2.7)
4.0 (3.7–4.6)
a
Estimated by inverse prediction of host egg age (days) with normal logistic regression model at 75, 50, and 25 % of the observed host eggs not being utilized (or attacked) by Oobius agrili. All logistic regression models for different treatment temperatures showed significant relationship between host egg age and the probability of the host eggs not being attacked by O. agrili (likelihood ratio tests: P \ 0.0001 for all tests)
development to adults (v2 = 87.14, df = 3, P \ 0.0001), diapause (v2 = 183.29, df = 3, P \ 0.0001) and mortality (v2 = 25.03, df = 3, P \ 0.0001) of immature O. agrili. When data from the highest test temperature (35 °C) were excluded from the logistic
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regression model, no significant effects of temperature were detected on any of these parameters (development to adults: v2 = 2.47, df = 2, P = 0.1181; diapause: v2 = 2.43, df = 2, P = 0.2594; mortality: v2 = 4.51, df = 2, P = 0.1047).
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Fig. 2 The relationship between host egg suitability (HT50 values predicted with the logistic model) and exposure temperatures
Fig. 4 Cumulative probability of an adult wasp emerging (event) in relation to rearing temperatures
P \ 0.0001). The point estimates of median time by individual survival curves for 50 % of immature O. agrili emerging to adults at 20, 25, and 30 °C were 38, 18, and 17 days after parental wasp oviposition, respectively (Fig. 4). Survival analyses further indicated that there were also significant differences in the time event of adult wasp emergence between any two temperature treatments (log-rank tests: all P \ 0.0005).
Discussion
Fig. 3 Effects of exposure temperatures on mean number of host eggs attacked by O. agrili in 24 h of exposure
Results from the survival analysis showed that temperature significantly affected time events of adult wasp emergence (log-rank test: v2 = 110.04, df = 3,
Results from our study showed that the window of host susceptibility (as measured by HT50 estimates) to O. agrili parasitism declined significantly from 14.1 to 2.3 days in an inverse second-order relationship with increases of exposure temperatures from 20 to 35 °C (Table 1; Fig. 2). In contrast, the parasitoid host attack rate changed in a bell-shaped second-order relationship—i.e., increased with treatment temperature from
Table 3 Development, diapause and mortality of immature O. agrili reared at different treatment temperatures Temperature (°C)
Na
% Developed to adults (±SE)b
% Diapaused (±SE)b
% Died (±SE)b
20
47
75.5 ± 11.6a
24.5 ± 11.6a
25
45
79.1 ± 10.4a
20.9 ± 10.4a
0 ± 0a
30
45
60.6 ± 6.71a
34.9 ± 7.76a
4.5 ± 2.78a
35
42
0 ± 0b
0 ± 0b
0 ± 0a
100 ± 0b
a
Total number of parasitized eggs (containing immature O. agrili) summed across five replicates of assays, each consisted of ten host eggs b
Mean (±SE) calculated with data from five replicates of assays for each temperature. Values with the same letter within the same column indicate no significant differences according to logistic regression analyses (p = 0.05)
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20 to 25 °C, but decreased at about the same rate when temperatures increased from 30 to 35 °C. This range of treatment temperatures also significantly affected the development and mortality of immature parasitoids with 35 °C resulting in 100 % mortality. While there was no significant difference in the percentage (20.9–34.9 %) of immature O. agrili that entered diapause (as mature larvae), with little (0–4.5 %) mortality at 20, 25, and 30 °C, there were significant differences in the time event of adult wasp emergence within this temperature range. The median time for 50 % of immature O. agrili emerging as adults at 20, 25, and 30 °C were 38, 18, and 17 days after parental wasp oviposition, respectively. Together, these findings indicate that temperature can profoundly influence host utilization patterns of the EAB egg parasitoid O. agrili. More importantly, the non-linear and unequal temperature effects on these host utilization parameters are likely to result in differential host parasitism rate and thus affect the efficacy in suppressing host populations in the future. However, it should be noted that in our experiments temperatures were kept constant throughout, but in the field daily and seasonal variability in temperature will also likely be important (Musolin et al. 2010). In North America, EAB females lay their eggs underneath bark flakes or in small crevices on the trunks of ash trees in late spring-early summer (Herms and McCullough 2014). EAB eggs typically take 1–3 weeks to develop and their development time is inversely related to temperature (Duan et al. 2013). For example, no EAB eggs hatch at 12 °C, while at 20 °C it takes 20 days for eggs to complete development and at 35 °C only seven days (Duan et al. 2013). Our results showed that as temperature increases, the window of susceptibility of EAB eggs to O. agrili decreases. Thus, in warmer climates, EAB eggs will likely develop more quickly and have a shorter window of susceptibility to O. agrili parasitism. In addition to this shorter window of susceptibility, we found that the attack rate of O. agrili on EAB eggs increases at lower temperature range (20–25 °C), but decreases at about the same rate at higher temperature range (30–35 °C). While insect activity generally increases with temperature (Gilbert and Raworth 1996), our data suggest that O. agrili attack rate should peak between 25 and 30 °C (Fig. 3). Such behavior is not uncommon among hymenopteran parasitoids, with other studies also indicating that
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some species show a decrease in attack rate between 25 and 30 °C (Mbata et al. 2005; Zamani et al. 2006). Therefore, in combination, our results show that at lower temperatures, EAB eggs are susceptible to O. agrili for a longer period of time which compensates for a lower attack rate. However, at higher temperatures above 30 °C, both the window of susceptibility and the attack rate decrease. Thus, higher temperatures (above 30 °C) would inevitably result in reduction of the efficacy of O. agrili in biological control of EAB. In the event that EAB eggs are parasitized, the optimal temperature for the development and survival of immature O. agrili appears to be around 25 °C with slightly increased mortality at 30 °C and complete mortality at 35 °C. There was little difference in the median development time of immature O. agrili at both 25 and 30 °C (18 and 17 days, respectively), which indicates that this parasitoid might be able to complete more generations per year in warmer climates. It was also interesting that there was a relatively consistent portion of the parasitoid population that entered diapause, regardless of the treatment temperature in the range of 20–30 °C. More work is needed to determine if this diapause is a founder effect from the original population of O. agrili collected, or if it is a plastic response to the environment that can change after multiple generations. Increased temperature could also have effects on progeny beyond what was quantified in our experiments. For example, Wu et al. (2011) found that larvae of the parasitoid Aphidius colemani (Hymenoptera: Braconidae) were smaller when reared at 25 °C in comparison to when reared at 15 °C. Overall, findings from the study suggest that O. agrili might not be well suited to areas towards the southern extent of the current EAB range in North America, and under future climate change this could extend further north (Liang and Fei 2014). Although there are many factors that would contribute to the successful establishment of O. agrili (such as host density and number of parasitoids released), mean high temperatures could in part explain why this parasitoid appears to have thus far been more successful in the Midwest compared to the midAtlantic regions of the United States. EAB is likely to continue to expand its range in North America, with human-assisted movement (e.g., movement of firewood) enabling the beetle to disperse rapidly (Muirhead et al. 2006; Prasad et al. 2010; Sobek-Swant et al.
Biological control of an invasive forest pest
2012). Anecdotal evidence from release sites suggests that O. agrili is relatively slow to disperse, and it is possible that incongruence in ranges between parasitoid and host could occur. However, if EAB larvae are transported via firewood, it follows that parasitized EAB eggs may also disperse this way. Results from the present study highlight the need to incorporate data on multiple aspects of species biology when attempting to draw general conclusions regarding their potential response to climate change. For example, if just considering the development time of O. agrili, it would appear as though this species would respond positively to a warmer climate. However, once the host window of susceptibility and parasitoid attack rate are taken into consideration (Figs. 2, 3), it is clearer that O. agrili will likely respond negatively to a warmer climate with average high temperature above 30 °C, particularly the extreme heat due to global warming in the summer months when the parasitoid needs to synchronize with the presence of their host eggs. The current range of O. agrili in China may further support our conclusion that hot temperatures (particularly extreme heat) may be one of the key factors limiting its distribution. For biocontrol of EAB in North America, we thus suggest that this parasitoid should be released in colder climate zones such as northeast and Midwest United States and Canada, and perhaps not in more southern states such as Tennessee. Acknowledgments We thank Jacqueline Hoban and Susan Barth (University of Delaware) for their great assistance in all phases of the study. We appreciate the assistance of Dick Bean, Kim Rice, and Charles Pickett (Maryland Department of Agriculture) in producing and shipping adult EAB to us for this study. Jonathan Lelito (USDA-APHIS, Brighton Emerald Ash Borer Biocontrol Lab) provided some adult parasitoids (originally collected from Jilin Province, China) for tests with host attack rates. We are also grateful to Roger Fuester and Doug Luster (USDA-ARS, Beneficial Insects Introduction Research Unit) for helpful comments on an earlier version of the manuscript.
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Jian J. Duan is a research entomologist and lead scientist with the U.S. Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit. His research focus is on biological control of invasive wood-boring pests such as emerald ash borers, which involves (a) natural enemy exploration, importation, quarantine safety testing, and non-target risk assessment; (b) ecological and behavioral studies on host habitat/and host utilization patterns of introduced natural enemies, (c) development spatial and temporal population dynamic models to predict the colonization, establishment, and distribution of imported natural enemies in their region of new introduction. David E. Jennings is a postdoctoral research associate at University of Maryland. His research interest is in biological
Biological control of an invasive forest pest control of agricultural and forest insect pests, and has been working on biological control of emerald ash borer since 2011. Dontay C. Williams was a U.S. Department of Agriculture student intern funded by USDA Student Career Enhancement Program, and has currently earned his master degrees in science from University of Arkansas.
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Kristi M. Larson is a research associate at University of Delaware and has been working on biological control of emerald ash borer since 2011.
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