PHYSIOLOGICALANDCHEMICALECOLOGY Temperature-Dependent Development Rate of doryphorae (Diptera: ) within Its Host, the (Coleoptera: Chrysomelidae)

ROLANDO L6PEZ, DAVID N. FERRO, ANDJOSEPH S. ELKINTON Department of Entomology,Universityof Massachusetts,Amherst, MA 01003 Downloaded from https://academic.oup.com/ee/article/26/3/655/418275 by UMass Amherst Libraries user on 16 March 2021

Environ. Entomol. 26(3): 655-660 (1997) ABSTRACT Myiophanls donjphorae (Riley), a tachinid parasitoid of the Colorado potato beetle, were reared at a 27°C constant temperature after being deposited within 2nd-instar beetle larvae. Their growth was measured 48 and 96 h after larviposition. During this time, M. doryphorae larvae grew but remained as 1st instars while the parasitized beetle larvae reached full maturity and dropped to the ground to pupate. The development rates of para- sitized 3rd-instar Colorado potato beetle larvae and the parasitoids within them in 1990 and 1991 were measured at 6 and 5 different constant temperatures, respectively.M. doryphorae development rate was measured for the interval between late Ist-instar larvae until adult emergence. These data were fitted to the nonlinear, temperature-driven rate of development model of Hilbert and Logan.

KEY WORDS Myiophanls donjphorae, Leptinotarsa decemlineata, development rate, host, parasitoid

TIm RELATIONSHIPBETWEENtemperature and in- velopment rates, principally in the middle ranges sect development has long been recognized (San- of applicable temperatures. Here we use the mod- derson and Peairs 1913, Uvarov 1931, Davison el of Hilbert and Logan (1983) which is described 1944, Richards 1957, Howe 1967, Gilbert and Ra- by r (T) = P [ (T2j (T2+ D2)) - e-(Tm-T)/8I'] where worth 1996) as an important environmental param- r(T) is the rate of development at temperature T; eter in modeling population dynamics. De- T= To - Tb where To is the air temperature and velopment rate is defined as the reciprocal of the Tb is the developmental base temperature; Pis the time required to complete the egg, larval, or pupal developmental rate at the base temperature Tb; stages (Campbell et aI. 1974). Accurate estimates Tm (defined above); D is a shape parameter that of the development rate of insect pests and their controls the inflection point of the sigmoid curve natural enemies are of obvious significance in the (it is an empirical parameter); and 8f is the tem- development of control programs; during the past perature range between developmental maximum decade the use of phenological models in inte- and Tm. grated pest management programs has increased The Hilbert and Logan' model has been more considerably (Wagner et al. 1984a; Worner 1991, realistic in not predicting growth at the low and 1992). Linear degree-day models were some of the high temperatures known to be lethal to the Col- earliest to be developed and were applied to a orado potato beetle (Ferro et al. 1985) unlike other large number of insect species (Howe 1967), but widely used nonlinear models such as those of Lo- the non-linearity of development found at high and gan et al. 1976 and Sharpe and DeMichele 1977. low temperatures demonstrated these models of- Based on this feature and on the success of this ten to be inaccurate in describing insect develop- model in describing Colorado potato beetle larval ment. A number of nonlinear models, some of and pupal development (Ferro et al. 1985, Logan them empirical (Logan et al. 1976, Hilbert and Lo- et al. 1985), the Hilbert and Logan model was cho- gan 1983) and others theoretical (Sharpe and sen for application in the current study to Myi- DeMichele 1977, Schoolfield et al. 1981) have opharus doryphorae (Riley), an important parasit- been elaborated for a wide variety of species and oid of the Colorado potato beetle in North circumstances; further work (Hilbert and Logan America. 1983, Wagner et al. 1984a, b, Gould and Elkinton With very few exceptions (Nealis et al. 1984, 1990, Hebert and Cloutier 1990,) has applied and Gould and Elkinton 1990), these nonlinear tem- evaluated these models. perature-dependent growth models have been Among the nonlinear models referred to above, used to describe the development of single, non- most have been found reliable in describing de- parasitic insect species. No temperature-related

0046-225X/97/0655-0660$02.00/0 © 1997 Entomological Society of America 656 ENVIRONMENTAL ENTOMOLOGY Vol. 26, no. 3 development rate studies have been conducted on foliage was provided daily as food for the beetle M. doryphorae. First summer adults of M. dory- larvae. Twenty-five of the parasitized larvae were phorae larviposit into Colorado potato beetle lar- dissected after 48 h and the other half after 96 h. vae (mainly Ist-3rd instars) (Tamaki et al. 1983). In all cases, the lengths of the parasitoid larvae The parasitoid larva kills its host at the prepupal were measured immediately. Using these measure- stage and completes its development within this ments, the growth of the parasitoid 1st instars stage. The 2nd parasitoid summer generation also within 3rd- and 4th-instar Colorado potato beetle attacks hosts (lst-3rd instars) (Kelleher 1960). was regressed on the number of hours since lar-

However, some of the parasitoids deposited by this viposition using both a linear model and a qua- Downloaded from https://academic.oup.com/ee/article/26/3/655/418275 by UMass Amherst Libraries user on 16 March 2021 generation allow their host larvae to complete de- dratic regression model (Sigmaplot 1994). velopment and enter diapause while parasitoid lar- Temperature-Dependent Development of vae remain undeveloped within the diapausing Colorado Potato Beetle and Myiophams spp. host. They do not complete their development un- Colorado potato beetle adults and Myiophams til their hosts emerge the following spring (L6pez spp. used in this experiment were collected in et al. 1992). In both M. doryphorae generations, July and August 1990 from a potato field (Katah- parasitoid development occurs entirely within the din) located at the University of Massachusetts host. Because of the complex relationship between Vegetable Research Farm, South Deerfield, MA, the host physiology and the parasitoid larvae for and maintained under greenhouse conditions (25 the overwintering generation, the summer gener- ± 3°C, 80% RH, and a constant photoperiod of ation of M. donjphorae was selected for evaluation 16:8 L:D h). of temperature-dependent development. During 1990, the Colorado potato beetle larvae It has been known for some time that M. do- may have been parasitized by either M. dorypho- nJphorae remain as Ist-instar larvae throughout rae or Myiophams aberrans (Townsend), and it the larval development of their Colorado potato was not possible to discriminate among parasitized beetle hosts (Trouvelot 1931, Kelleher 1960, Ta- larvae by parasitoid species. Therefore, in 1991 the maki et al. 1983). Some authors have taken this to experiment was repeated using only M. dorypho- mean that no parasitoid growth occurs during this rae. time, although Kelleher (1960) reported an aver- From the 1st progeny of beetles, 360 third in- age difference in length of 0.64 mm between re- stars in 1990 and 300 in 1991 were exposed to cently laid Ist-instar M. doryphorae larvae and fertile Myiophams spp. flies until each larva had presumably older Ist-instar parasitoids found in been parasitized (L6pez et al. 1992). All of the par- mature (4th instar) Colorado potato beetle larvae. asitized Colorado potato beetle larvae were kept in An initial aspect of this project was to establish the greenhouse in ventilated plastic containers (7 whether 1st instars grow while in its larval host by 7 by 14 cm); foliage was placed on top of a 2-cm before the host pupates. The 2nd aspect was to layer of moistened vermiculite which covered the model the temperature-dependent development of bottom of each container as a substrate for the summer-generation M. doryphorae within prepu- prepupae. In total, 10 Colorado potato beetle lar- pal Colorado potato beetle. vae were left in each container. Excised potato leaf- lets were provided by inserting the stem into a floral water pic containing quarter-strength Hoagland's Materials and Methods solution (Hoagland and Amon 1950); potato fo- Myiopharus doryphorae Larval Growth from liage was then placed within each container and Larviposition to Completion of Host Larval De- changed every day until Colorado potato beetle velopment. Early 3rd-instar Colorado potato larvae completed their development and entered beetle larvae from a laboratory colony were ex- the vermiculite to pupate. posed to 5 fertile M. doryphorae in a Plexiglas- Another 360 Colorado potato beetle 3rd instars framed and metal screen cage (35 by 35 by 35 cm) in 1990 and 300 in 1991 not exposed to the flies under laboratory conditions. After each Colorado were kept under the same conditions as the para- potato beetle larva was parasitized (L6pez et al. sitized larvae and were used as controls. At the 1992), the larva was immediately removed from onset of Colorado potato beetle pupation, prepu- the cage using soft tweezers and placed in a plastic pae from each group (parasitized and not parasit- petri dish (25 by 5 mm) with fresh potato foliage ized) were left in the same containers (60 larvae until 75 parasitized larvae were obtained. Twenty- per container) in which they were reared, and the five of the parasitized Colorado potato beetle lar- containers were placed in each of the growth vae were dissected immediately after parasitiza- chambers maintained at 17, 20, 24, 27, 30, and tion, and the length of the M. dOT'lJphoraelarvae 32°C in 1990, and at 20, 25, 28 30, and. 32°C in found within them was recorded. The remaining 1991. All chambers were kept at a 16:8 (L:D h) 50 parasitized Colorado potato beetle larvae were photoperiod and 80% RH. The containers were separated into 2 groups of 25 each and placed in kept in the chambers until emergence of adult a growth chamber maintained at 27°C and 80% Colorado potato beetles and Myiophams spp. RH. At 27°C, 3rd-instar Colorado potato beetle The Hilbert and Logan Model described (Hil- larvae molt to the 4th instar in 3-4 d. Fresh potato bert and Logan 1983) was fit to values of the geo- June 1997 L6PEZ ET AL.:TEMPERATURE-DEPENDENTDEVELOPMENTOF Myiopharus doryphorae 657

1.8 (mean :!:: SE) long for recently laid parasitoid lar- - Qua,lnltic regression vae, 1.01 :!:: 0.02 mm long after 48 h, and 1.14 :!:: e I.S ...... 95% Confidence interval 0.061 mm long after 96 h. It takes =96 h for Col- .§. orado potato beetle larvae raised at 27°C to go from late 3rd instar to the prepupal stage (Wal- j 1.2 ...... •...... genbach and Wyman 1984, and Ferro et al. 1985, Logan et. al. 1985). A quadratic regression was fit 0.9 to all data points. The quadratic regression Y = i 0.698 + 0.422 x - 0.115 x2 (,,2 = 0.767) fit Myi- Downloaded from https://academic.oup.com/ee/article/26/3/655/418275 by UMass Amherst Libraries user on 16 March 2021 '!l 0.6 opharus spp. Ist-instar larval growth (Fig. 1). The fitted curve indicated a steady growth of the Myi- ·a y ~ 0.698 + 0.422<- 0.115'; opharus 1st instars from 0 to 48 h after larviposi- H 0.3 .'-0.767 tion and from 48 to 96 h, the rate of growth ap- " peared to stabilize and there was no further size 0.0 0 48 96 increase until the beetle larvae reached the pre- Houl1l after larviposition pupal stage (Fig. 1). This result supports the study of Kelleher (1960), which showed that 1st instar Fig. 1. Quadratic regression for M. doryphorae Ist- Myiopharus spp. doubled its size (body length) instar larval growth before Colorado potato beetle reached prepupal stage. within the Colorado potato beetle larva before the beetle larva reached the prepupal stage. Myiopha- rus larvae do not molt to the next instar until its metric mean rate of development at each temper- host larva drops to the ground to pupate. ature which was calculated as mean developmental Temperature-Dependent Development of rate = lIexp[Iln (D;)/ n] where Dj is the observed Colorado Potato Beetle and Myiophants spp. developmental time and n is the sample size. Mean Parameter values for the Hilbert and Logan model developmental rates were computed in this way to (defined above for the 1990 experimental data) correct for the skewed frequency distributions of were estimated by the Marquardt nonlinear least developmental time (Logan et al. 1976). squares with the function fit to data in Tables 1 Initial estimates of the 4 parameters were de- and 2. The sum of squares caused by errors (SSE) termined graphically as described in Logan et al. is an estimate of the fit of the model. The smaller (1976). Nonlinear regression (SAS Institute 1988) the SSE, the better the fit. The parameters for was used to fit the model to values of mean de- Myiopharus spp. were Tb = 2.36525; D = 86.3803; velopment rate by an iterative least-squares pro- 'I' = 1.2688; T m = 34 ; and 5T = 1.1072 with SSE cedure using the Marquardt algorithm (Marquardt = 0.000162, and for Colorado potato beetle the 1963). For the Marquardt nonlinear least squares, parameters were Tb = 2.26751; D = 83.52402; 'I' 250 iterations were chosen because it has been = 1.18252; Tm = 34; and 5T = 1.0949 with SSE shown from our experience that after that number = 0.000162 for 1990. Fig. 2 presents the empirical of iterations, in most cases the parameter values data and the fitted curves for 1990 and 1991. The change very little. parameter values in 1991 were fit to data in Tables 1 and 2 for M. doryphorae and Colorado potato beetle, respectively. The parameters for 1991 for Results and Discussion M. doryphorae were Tb =4.55643; D = 89.963020; Myiophants doryphorae Larval Growth from 'I' = 1.530223; T m = 34; and 5T = 1.951225 with Larviposition to Completion of Host Larval De- SSE = 0.000021958, and for Colorado potato velopment. M. doryphorae larvae raised at a con- beetle the parameters were Tb = 3.873746; D = stant temperature of 27°C during the larval devel- 106.87168; 'I' = 2.36702; T m = 34; and 5T = opment of their hosts were 0.69 ± 0.021 mm 1.4855 with SSE = 0.00008298. The development

Table 1. Development of Myiopharus sp. (1990) and M. doryphorae (1991) at different constant temperature regimes

Parameters Myophams sp .. 1990 M. doryphome, 1991 Temperature, °C 17 24 27 30 34 20 25 28 30 32 Mean development time, d 38.3 15.1 12.7 12.0 11.0 28.6 16.5 14.4 12.1 14.1 SE 0.8 0.3 0.3 0.1 0.0 0.5 0.3 0.2 0.3 0.2 No. 60 60 60 60 60 60 60 60 60 60 No. not completing development 7 10 5 9 58 0 0 4 4 18 Development rate/d 0.03 0.07 0.08 0.08 0.08 0.04 0.08 0.09 0.1 0.08

Host stage, prepupa-pupa; parasitoid stage, larva-pupa. 658 ENVIRONMENTAL ENTOMOLOGY Vol. 26, no. 3

0.14

• CPB 1990 CPBmodel 0.12 • Myiopharus sp. - - Myiopharus sp. model 0.10 Downloaded from https://academic.oup.com/ee/article/26/3/655/418275 by UMass Amherst Libraries user on 16 March 2021

0.08

0.06

0.04

0.02 0.16 CPB • CPB model 1991 •....• I v Myiopharus doryphorae tI:l 0.14 ~ - - Myiopharus doryphorae model "'0 • 0.12 ~•... -=cu 0.10 c..e 0 QS i) 0.08 Q 0.06

0.04

0.02 16 18 20 22 24 26 28 30 32 34 36 Temperature (0 C)

Fig. 2. Temperature-dependent development rates of Colorado potato beetle prepupa to adult and Myiopharus sp. late 1st instar to adult emergence as a nonlinear model of each. rate using the Hilbert and Logan (1983) equation 0.000021958 for Myiopharus spp. and SSE = projects to 0 at T~Tb' The sum-of-squares errors 0.00008298 for Colorado potato beetle. in 1990 indicated a similar fit of the cUlVe to the The empirical nonhnear model of Hilbert and values for both Colorado potato beetle and Myi- Logan (1983) predicted a lower temperature opharus spp. (SSE = 0.000162). The SSE for the threshold for development of both Colorado po- 1991 data indicated a much better fit for both the tato beetle and Myiopharus than has normally host and the parasitoid. However, the fit seems to been assumed (Tb = lOOC for most ); the be shghtly better for Myiopharus than for the Col- predictions of the model were Tb = 4.56°C for orado potato beetle, with values of SSE = Myiopharus and Tb = 3.87°C for the beetles. June 1997 LOPEZET AL.:TEMPERATURE-DEPENDENTDEVELOPMENTOF Myiophams doryphorae 659

Table 2. Development of Colorado potato beetle pupa at constant temperature regimes, 1990-1991

Parameters 1990 1991 Temperature.oC 17 24 27 30 34 20 25 28 30 32 Mt'an dt'wlopnlt'nt tillle. d 30.3 12.5 11.6 8.4 9.3 22.3 15.1 11.3 9.8 lUI 51<: 0.8 0.4 0.3 0.1 0.1 0.4 0.3 0.3 0.3 0.] No. 60 60 60 60 60 60 60 60 60 60 No. not t'omplt'ting dt'\'..Jopment 0 6 ]8 0 2 0 0 0 0 5 Downloaded from https://academic.oup.com/ee/article/26/3/655/418275 by UMass Amherst Libraries user on 16 March 2021 Development rate/d 0.03 0.08 0.09 0.]2 O.ll 0.06 0.08 O.ll 0.]3 0.1]

Jn all cases, stage is prepupa-pupa.

These values may be correct in spite of the diffi- emergence when both were reared under the same culty to show empirically any growth at tempera- environmental conditions. hues between 4 and 10°C. There was less vari- The focus of this study was on the 2nd period ability in development rates at higher of Myiopharus spp. development and it was mod- temperatures, at least up to those of maximum de- eled as a function of temperature. To improve the velopment, than at lower temperatures. The Hil- fit of the model during this growth period, more bert and Logan model appeared to be more reli- experimental data covering the temperature range able than earlier models. It predicted the decline from 7 to 15°C are needed. The developmental in growth as temperatures exceeded the tempera- rate curves described herein for Colorado potato ture where maximum growth occurred. Our results beetle and Myiophams are based on the Hilbert using the Hilbert and Logan model showed the and Logan (1983) model and appear to be a work- Colorado potato beetle pupal development rate able tool for temperatures from 15 to 32°C. The reaching its maximum at 29°C whereas Ferro et al. M. doryphorae stage that we modeled coincides 1985, using an earlier version of the model (Logan with the development conditions of the 2nd sum- et. al. 1976), showed the pupal development rate mer generation that normally emerges in Massa- of the Colorado potato beetle reaching its maxi- chusetts in mid-July and attacks the 2nd-genera- mun at 28°C. However, this minor discrepancy tion beetle larvae. Many of the parasitoid larvae comes within acceptable experimental error. deposited in host larvae from the 2nd week of Au- In spite of many valid criticisms (Womer 1991, gust until the end of the summer will remain un- 1992) regarding the possible inaccuracies of non- developed and overwinter within their adult host. linear models using constant temperatures versus They do not complete their development until af- variable temperatures and under laboratory versus ter the beetle emerges the following spring (Lopez natural conditions, there still exists a need to pre- et al. 1992). From the current study, it is clear that dict population growth trends of both host and the summer generation of the parasitoid seems to parasitoids for a variety of conditions for which no be well synchronized with host availability; that is adequate alternative methods exist for measuring precisely what it is observed in potato fields in such growth. Our findings indicate that Myiopha- western Massachusetts. However, the overwinter- ms summer-generation development includes 2 ing generation misses almost the entire 1st gen- periods, the 1st when parasitoid larvae are recently eration of the host as a trade-off for surviving as a laid and before their host larvae reach the prepu- larva within the adult overwintering host. For this pal stage, and the 2nd between the host prepupal reason, M. doryphorae has been catalogued in the stage and adult Myiopharus emergence. Several past as an asynchronous parasitoid of the Colorado other factors besides temperature seem to be act- ing upon the physiology of Myiophams affecting potato beetle (Kelleher 1960, Tamaki et al. 1983). their rate of development during each of these pe- A study on the development rate of the overwin- riods. From a practical viewpoint, the 1st period tered parasitoid after beetle emergence in the of Myiopharus growth seems to be host-dependent spring would significantly improve our understand- rather than temperature-dependent. When same- ing of the relationship between M. doryphorae and aged hosts are parasitized at different instars dur- Colorado potato beetle. ing their larval development, all adult parasitoids seem to emerge at about the same time (Tamaki Acknow1edgment8 et al. 1983). The 2nd period also was indirectly host-dependent in that parasitoid larval develop- We thank Craig Stevens and Rolf Parker for field and ment did not begin until the host entered the pre- laboratory assistance. Jesse Logan and R. Hilbert were pupal stage. Once the parasitoid development was very helpful providing information about their model. triggered, development was temperature-depen- This research was supported by Massachusetts Agricul- dent, closely following their host development with tural Experiment Station, Project NE-178, Publication adult parasitoids emerging 1-2 d after beetle No. 3194. 660 ENVIRONMENTAL ENTOMOLOGY Vol. 26, no. 3

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