Temperature Effect on Postdiapause Development and Survival of ...

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ARTHROPOD BIOLOGY

Temperature Effect on Postdiapause Development and Survival of Embryos of Three Species of Melanoplus (Orthoptera: Acrididae) JAMES R. FISHER Rangeland Insect Laboratory, USDA-ARS-Northern Plains Area, Montana State University, Bozeman, MT 59717

Ann. Entomol. Soc. Am. 87(5): 604-608 (1994)

ABSTRACT Postdiapause development and survival of embryos to hatch were studied at 10 constant temperatures (12, 15, 18, 24, 27, 30, 33, 36, 39, and 42°C) for three species of North American grasshoppers: Melanoplus sanguinipes (F.), M. bivittatus (Say), and M. differentialis (Thomas). M. sanguinipes and M. bivittatus had similar development curves (rate versus temperature) with developmental thresholds of 10.4 and 9.8°C, respectively. M. differentialis had a slower development curve, but the developmental threshold was 8.8°C. Even though M. differentialis had a lower developmental threshold, mean hatch days, the time to the first day of hatch, and the respective thermal units were nearly double those of M. sanguinipes or M. bivittatus. Percentage of hatch was greatest at 26.8°C for M. sanguinipes, at 24°C for M. bivittatus, and at 26.3°C for M. differentialis; thermal death points were reached at 43, 42, and 42.3°C, respectively. KEY WORDS grasshoppers, hatch, development

THREE OF THE MOST economically important

species of grasshoppers that affect rangeland and crops in North America are Melanoplus sanguinipes (F.), M. bivittatus (Say), and M. differentialis (Thomas). All three species complete embryonic diapause sometime during the winter and begin postdiapause development as the soil begins to warm in the spring (Burdick 1937, Shotwell 1941, Salt 1949, Church & Salt 1952). Of these species, M. bivittatus and M. sanguinipes hatchlings usually appear in fields at nearly the same time (Shotwell 1941). Hatchlings of M. differentialis appear 2—4 wk later. Like most North American Acrididae, these three species overwinter in the egg stage and, presumably, have an embryonic diapause. The diapause is completed by spring (Shotwell 1941) or after 3 mo in a refrigerator (Henry 1985). If ample time is allowed for diapause termination, it is possible to describe postdiapause development and survival at many different constant temperatures. Temperature is the driving variable in the springtime hatch of these species, and thermal developmental thresholds for their eggs have been estimated but have not been conclusive (Parker 1930, Burdick 1937, Shotwell 1941, Church & Salt 1952, Uvarov 1966, Randall & Mukerji 1974, Hewitt 1985, Onsager 1986, Kemp & Sanchez 1987). In this article, I describe the postdiapause developmental rates and the thermal thresholds for postdiapause eggs of M. sanguinipes, M. bivittatus, and M. differentialis. In

addition, optimal ranges for development and thermal limits are described for consideration when rearing these species. Materials and Methods Egg Origin and Preparation. Egg pods were obtained as described by Henry (1985) from laboratory and greenhouse rearings of M. sanguinipes, M. bivittatus, and M. differentialis collected in Montana. They were placed with moistened vermiculite in small plastic containers, 50 pods per container, for 30 d at room temperature (24 ± 3°C) to allow the embryos to reach the diapause stage (Salt 1949, Riegert 1961, Henry 1985). Containers with pods were then placed in a refrigerator (3.5-8.0°C) for 5 mo to allow diapause completion; 5 mo is more than sufficient to terminate diapause (Bodine 1925, Parker 1930, Church & Salt 1952, Henry 1985). After refrigeration, the eggs were removed from the pods. Ten healthy eggs (cream-colored to light brown and robust) were selected randomly from broken pods and were placed on moistened, fine-sieved ( - 1). eo.oo73 70% and where postdiapause development progresses rapidly. Using the number of eggs hatched per species per temperature, a best-fit polynomial regression (NCSS [Hintze 1990]) was used to estimate the OTR and to estimate the maximal thermal limit (TDP) or thermal death point temperatures (maximum x intercept). The coefficients of this regression were used to calculate maximal hatch (the ultimate point of the parabola) and the optimal hatch temperature (OTH) (Zar 1984): OTH = bJ2 b2; and maximal hatch (MH) MH = a - (bj*/4b2). The regression had the form of the quadratic, y = 2

Results Development Rates and Hatch. M. sanguinipes and M. bivittatus had similar developmental rates (Fig. 1). The calculated DT (y = 0) for M. sanguinipes from the model (Fig. 1A), rate (T) = e 0 0 0 6 6 (T " 1 0 4 2 ) - 1, r 2 = 0.995, error sum of squares (ESS) = 27.20, (T = a particular temperature), was 10.42°C. The rate of development for M. bivittatus was estimated by the model, rate (T) = e 0 0 0 7 3 (T " 9 7 7 ) - 1, r 2 = 0.997, ESS = 6.60 (Fig. IB), with the DT estimated as 9.8°C. M. differentialis had a lower DT, 8.81°C, determined from the rate model, rate (T) = e0.00329 (T - 8.81) - \ ^ = Q.997, ESS = 12.4 (Fig. 1C). Day to first hatch and mean hatch (days) were similar for M. sanguinipes and M. bivittatus over the various constant temperatures (Tables 1 and 2). Even though thermal unit accumulations were the same (Tables 1 and 3), M. bivittatus, at a majority of temperatures, required fewer days for hatch, which may be biologically significant. However, it should be noted that the calculated

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Table 1. First hatch day and related thermal units and mean hatch day and related thermal units for each species studied over all constant-temperature treatments Species Melanoplus sanguinipes Melanoplus bivittatus Melanoplus differentialis

First hatch Thermal Mean hatch Thermal day" unitsb dayc unitsd

Table 3. Thermal unit calculations (per day) for first hatch day and mean hatch day for eggs of Melanoplus sanguinipes, M. bivittatus, and M. differentialis when held at 10 different constant-temperature regimes Te mp ' o

Hatch

First Mean First Mean First Mean First Mean First Mean First Mean First Mean First Mean First Mean First Mean

17.97a

136.11a

20.12a

157.44a

12

15.47a

135.03a

18.30a

158.16a

15

21.02b

294.18b

22.71b

325.36b

18

Numbers in the same column followed by the same letter are not significantly different from each other (P = 0.05) according to the studentized maximum modulus test (SAS Institute 1988).

24

" ANOVA, F = 399.91; df = 2, 748; P > 0.0001. b ANOVA, F = 956.08; df = 2, 748; P > 0.0001. c ANOVA, F = 472.16; df = 2, 748; P > 0.0001. d ANOVA, F = 1525.38; df = 2, 748; P > 0.0001.

27 30 33 36

threshold for M. sanguinipes was 10.4°C and that of M. bivittatus was 9.8°C. Thermal unit calculations and first hatch and mean hatch for M. differentialis were greater than double those of either of the other two species (Tables 1 and 2). Less than 15% of M. sanguinipes hatched at 12°C, and only 0.77% hatched at 42°C (Table 2). M. bivittatus had 38% hatch at 12°C, but no emTable 2. First hatch (days), mean hatch (days), and total number of eggs that hatched when eggs of Melanoplus sanguinipes, M. bivittatus, and M. differentialis were held at 10 different constant-temperature regimes Temp, °C 12 15 18 24 27 30 33 36 39 42

0

Hatch

M. sanguinipes

M. bivittatus

M. differentialis

First Mean" Hatch* First Mean Hatch First Mean Hatch First Mean Hatch First Mean Hatch First Mean Hatch First Mean Hatch First Mean Hatch First Mean Hatch First Mean Hatch

65.23 ±8.11 69.95 ± 8.03 44 32.37 ± 0.83 36.06 ± 0.69 109 16.43 ± 0.63 20.03 ± 0.65 192 12.00 ± 0.00 12.42 ± 0.14 176 9.16 ± 0.39 12.00 ± 0.19 228 5.13 ± 0.06 6.34 ± 0.17 213 5.63 ± 0.13 7.21 ± 0.15 268 5.70 ± 0.30 6.28 ± 0.43 102 4.03 ± 0.03 4.49 ± 0.17 161 6.00 ± 0.00 6.00 ± 0.00 2

59.57 ± 1.67 67.97 ± 1.98 114 21.73 ± 0.33 28.96 ± 0.67 168 17.17 + 0.31 18.56 ± 0.20 250 9.03 ± 0.03 12.46 ± 0.84 183 7.07 ± 0.07 8.45 ± 0.26 226 6.00 ± 0.00 7.83 ± 0.58 186 5.00 ± 0.00 5.54 ± 0.14 233 6.44 ± 0.35 7.01 ± 0.39

99.25 ± 4.25 99.25 ± 4.25 4 47.30 ± 2.17 48.98 ± 2.21 59 33.17 ± 0.55 35.56 ± 0.56 254 19.20 ± 0.28 21.01 ± 0.16 243 15.80 ± 0.56 17.71 ± 0.28 231 12.47 ± 0.09 13.82 ±0.11 258 10.14 ± 0.11 11.70 ± 0.14 239 12.07 ± 0.07 12.32 ± 0.14 132 10.86 ± 0.20 13.55 ± 0.46 99 0 0 (-)

1 lclLv.ll

85

6.00 ± 0.00 6.06 ± 0.06 71 0 0 (-)

Mean ± SEM, based only on those eggs that hatched. Total number of eggs that survived to hatch from 300 eggs per regime (10 eggs x 30 replications). b

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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

39 42

M.

sanguinipes" 140.5 ± 150.7 ± 148.2 ± 165.1 ± 124.6 ± 151.8 ± 163.0 ± 168.7 ± 152.0 ± 192.3 ± 100.5 ± 124.1 ± 127.2 ± 162.8 ± 156.2 ± 172.3 ± 115.3 ± 128.2 ± 189.6 ± 189.6 ±

7.7 3.6 3.8 3.1 4.7 4.9 0.0 2.0 6.5 3.2 1.2 3.3 3.0 3.4 2.7 8.2 1.0 5.0 0.0 0.0

M. bivittatusb 132.8 dt 151.6 dt 113.6 db 151.5 dt 141.3 dt 152.7 dt 128.5 dt 177.3 dt 121.8 db 145.7 dt 121.4 db 158.3 dt 116.2 db 128.8 db 169.0 db 183.8 db 175.4 db 177.1 db

3.7 4.4 1.7 3.5 2.5 1.6 0.5 11.8 1.1 4.4 0.0 12.0 0.0 3.2 9.1 10.3 0.0 1.7

M. differentialis0 316.6 db 13.6 316.6 db 13.6 305.4 db 4.5 316.3 db 3.7 304.8 db 5.0 326.8 db 5.2 291.7 db 4.2 319.1 db 2.5 287.4 :t 10.1 322.1 db 5.0 264.2 db 2.0 292.8 :t 2.3 245.2 db 2.6 283.0 db 3.4 328.2 db 1.9 334.9 db 3.7 327.9 ± 6 . 1

409.0 ± 13.8

Numbers represent mean ± SD. ° Base temperature (M. sanguinipes), 10.4°C. b Base temperature (M. bivittatus), 9.8°C. c Base temperature (M. differentialis), 8.8°C.

bryos survived to hatch at 42°C (Table 2). Very few (4/300) M. differentialis embryos hatched at 12°C, and, as with M. bivittatus, no embryos survived to hatch at 42°C. Developmental Optima. For M. sanguini%ies the TDP (maximum x intercept) as calculated from the polynomial, % hatch = -127.43 (±9.80) + 15.25 (±0.80) t - 0.28 (±0.01) t2, r 2 = 0.56, P > 0.0001 (t = temperature, °C), was 43°C (Fig. 2A). The OTR was between 21 and 33°C with the OTH calculated to be 26.8°C with a MH of 77%. M. bivittatus hatch was described with the polynomial % hatch = -59.96 (±8.61) + 11.36 (±0.70) t - 0.24 (±0.01) t2, r2 = 0.62, P > 0.0001 (Fig. 2B). The TDP was calculated near 42°C with an OTH of 24°C and a MH of 76.2% at that temperature. For M. differentialis the TDP of 42.3°C and the OTH of 26.3°C were calculated from the polynomial % hatch = -144.71 (±6.10) + 17.37 (±0.53) t - 0.33 (±0.01) t2, r2 = 0.76, P > 0.0001 (Fig. 2C). The OTR was between 20 and 33°C, with a MH of 84% at 26.3°C. Discussion My results for time to hatch versus constant temperature regimes were similar to those of Parker (1930) for M. sanguinipes, of Shotwell (1941) for M. differentialis, and of Church & Salt (1952) for M. bivittatus for the few constant temperatures they studied. The days to hatch for M. bivittatus were somewhat longer than Shotwell (1941) described for similar regimes. The temperature regimes used by others (i.e., Parker [1930], Shotwell [1941], Church & Salt [1952])

FISHER:

607

Melanoplus POSTDIAPAUSE

B

C

/

0

10

20

30

40

TEMPERATURE (°C)

50 0

10

20

30

40

TEMPERATURE (°C)

50 0

10

20

30

40

50

TEMPERATURE (°C)

Fig. 2. Percentage hatch by constant-temperature regime (mean, ±SD) for (A) M. sanguinipes (hatch = •127.43 + 15.25t - 0.28*2), (B) M. bivittatus (hatch = -59.96 + 11.36* - 0.23*2), and (C) M. differentialis (hatch = •144.71 + 17.37* - 0.33*2).

were a sampling of temperatures within the temperature range for embryonic development of these insects, but they did not have a low temperature threshold nor a high temperature death point (lethal limit). By starting the intervals of temperatures at a sufficiently low temperature for some hatch (12°C) and ending at a sufficiently high temperature for high mortality (42°C), I was able to fit rate of development models to my data that exhibited high coefficients of determination. Shotwell (1941) stated that M. differentialis appeared later in the season than M. bivittatus because M. differentialis developed more slowly than M. bivittatus. My results support Shotwell's hypothesis (Fig. 1). The rate of development of M. differentialis at most temperatures was 0.3 to 0.5 that of M. bivittatus. Also, the rates of embryonic development for M. sanguinipes were the same as for M. bivittatus. However, casual observations by myself and others suggest that M. bivittatus (first instars [i.e., hatchlings]) appears in the field 3—4 d earlier than M. sanguinipes. Embryos of M. bivittatus had a lower developmental threshold than those of M. sanguinipes. M. bivittatus may have a slight developmental advantage over M. sanguinipes by developing earlier in the spring when temperatures are lower. In the field, hatch is also affected by oviposition behavior of different species (Kemp & Sanchez 1987, Fisher 1993). In addition, the OTH was 2.8°C higher for M. sanguinipes than for M. bivittatus, and the OTR for M. sanguinipes spanned a higher temperature range than the OTR for M. bivittatus. M. differentialis had an optimal temperature range and an optimal hatch temperature similar to those of M. sanguinipes and M. bivittatus (Fig. 2). Even though M. differentialis had a lower threshold of development and a much slower rate of growth than M. sanguinipes and M. bivittatus, it occurs in many areas with M. bivittatus

and M. sanguinipes. However, it has often been of greater importance as a pest in areas that have warmer and more humid summer conditions than in the rangeland areas of the northwestern United States. This species has been recorded as far north as southern Canada near the United States border (Pfadt 1989). It is possible that M. differentialis evolved in a more southern area of the continent than the other two species. This would offer a partial explanation for the prolonged development of the eggs. By having a slower embryonic growth rate, M. differentialis hatches in nearly all areas in a frost-free period and, thus, avoids the hazards often associated with hatch in late April to early May. Acknowledgments I thank biological laboratory technicians Philip Mazuranich and Connie Foiles and student aides Michael Ostenson II and William Johnson for their diligence and assistance with this study. Also, sincere thanks are extended to William P. Kemp (USDA-ARS), Jerome A. Onsager (USDA-ARS), Mark Carter (Colorado State University), Maria Marta Cigliano (Museo de La Plata, La Plata, Argentina), and two anonymous reviewers for their suggestions and critiques of early drafts of the manuscript. This work was supported in part by a cooperative agreement with the Grasshopper IPM Demonstration Program USDA-APHIS-PPQ, Boise, ID.

References Cited Bodine, J. H. 1925. Effect of temperature on rate of embryonic development of certain Orthoptera. J. Exp. Zool. 42: 91-109. Burdick, H. C. 1937. The effects of exposure to low temperature on the developmental time of embryos of the grasshopper Melanoplus differentialis (Orthoptera). Physiol. Zool. 10: 156-170. Church, N. S. & R. W. Salt. 1952. Some effects of temperature on development and diapause in eggs

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of Melanoplus bivittatus (Say) (Orthoptera: Acrididae). Can. J. Zool. 30: 173-184. Fisher, J. R. 1993. Location of egg pods of Aulocara elliotti (Orthoptera: Acrididae) in a field of crested wheatgrass in Montana. J. Kans. Entomol. Soc. 38: 416-420. Henry, J. E. 1985. Melanoplus spp., pp. 451-464. In P. Singh & R. F. Moore [eds.], Handbook of insect rearing. Elsevier, Amsterdam. Hewitt, G. B. 1985. Review of factors affecting fecundity, oviposition, and egg survival of grasshoppers in North America. U.S. Dep. Agric, Agric. Res. Serv. Bull. 36. Hintze, J. L. 1990. Number cruncher statistical system (NCSS), version 5.03. J. L. Hintze, Kaysville, UT. Kemp, W. P. & N. E. Sanchez. 1987. Differences in post-diapause thermal requirements for eggs of two rangeland grasshoppers. Can. Entomol. 119: 653651. Logan, J. A. & L. A. Weber. 1990. Population model design system (PMDS), version 5.0. Virginia Polytechnic Institute and State University, Blacksburg. Onsager, J. A. 1986. Stability and diversity of grasshopper species in a grassland community due to temporal heterogeneity. Proc. Panam. Acridol. Soc. 4: 101-109. Parker, J. R. 1930. Some effects of temperature and moisture upon Melanoplus mexicanus mexicanus

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Saussure and Camnula pellucida Scudder (Orthoptera). Mont. Agric. Exp. Stn. Bull. 223. Pfadt, R. E. 1989. Differential grasshopper. Wyo. Agric. Exp. Stn. Bull. 912. Randall, R. L. & M. K. Mukerji. 1974. A technique for estimating hatching of natural egg populations of Melanoplus sanguinipes (Orthoptera: Acrididae). Can. Entomol. 106: 801-812. Riegert, P. W. 1961. Embryological development of a nondiapause form of Melanoplus bilituaratus Walker (Orthoptera: Acrididae). Can. J. Zool. 39: 491-494. Salt, R. W. 1949. A key to the embryological development of Melanoplus bivittatus (Say), M. mexicanus mexicanus (Sauss.), and M. packardii Scudder. Can. J. Res. Sect. D Zool. Sci. 27: 233-255. SAS Institute. 1988. SAS/STAT user's guide, 6.03 ed. SAS Institute, Cary, NC. Shotwell, R. L. 1941. Life histories and habits of some grasshoppers of economic importance on the Great Plains. U.S. Dep. Agric. Tech. Bull. 774. Uvarov, B. 1966. Grasshoppers and locusts, vol. 1. Cambridge University Press, London. Zar, J. H. 1984. Biostatistical analysis, 2nd ed. Prentice-Hall, Englewood Cliffs, NJ. Received for publication 17 December 1993; accepted 28 April 1994.