Evidence of a Polymorphic Life Cycle in the , Adelges tsugae (Homoptera: )

MARK S. McCLURE Valley Laboratory, Connecticut Agricultural Experiment Station, Windsor, Connecticut 06095

Ann. Entomol. Soc. Am. 82(1): 50-54 (1989) ABSTRACT Hemlock woolly adelgid, Adelges tsugae Annand, has a polymorphic life cycle which involves hemlock, Tsuga, and , Picea. Studies in Connecticut revealed that Downloaded from https://academic.oup.com/aesa/article/82/1/50/16507 by guest on 29 September 2021 about half of the offspring produced by the sistens during June of two consecutive years became wingless adult progrediens. These closely resembled their mothers and remained on hemlock. The other half became winged adult sexupara and migrated to spruce where they produced eggs of the sexuales. However, none of the sexuales nymphs that hatched survived on any of 12 spruce species tested. Adelges tsugae, a cool-loving species, completed most of its development on hemlock from October through June. During the warm summer months, this aestivated as a first-instar nymph on the young branches at the base of the needles. All three generations of A. tsugae on hemlock had six stages of development, which included the egg, four nymphal instars, and the adult. Eggs and first-instar nymphs of the three generations were indistinguishable from one another. However, many of the later instars and the adults were readily distinguished from one another by the presence or absence of thoracic sutures and wing bud notches, by their degree of sclerotization, and by the size and shape of the body, thorax, and antennae.

KEY WORDS Insecta, Chermes funitectus, Picea, Tsuga canadensis

HEMLOCK WOOLLY ADELGID, Adelges tsugae An- I describe the life stages of this insect, including nand, is an important pest of Tsuga canadensis winged sexupara which migrate to spruce. Carriere in the eastern United States. First reported in eastern Virginia in the early 1950s, this adelgid Materials and Methods has spread primarily northeastward and now oc- curs as far north as Connecticut and Rhode Island Studies on the biology of A. tsugae were con- (Fig. 1). Adelges tsugae is undoubtedly an intro- ducted during 1986 and 1987 in two forests in duced species, but its homeland is unknown. It southern Connecticut. One site, located in Essex, occurs at low and innocuous densities in Formosa Middlesex County, was a mature forest of T. can- and in Japan (Takahashi 1937, McClure 1987). This adensis and mixed hardwoods heavily dominated adelgid also exists on Tsuga heterophylla Sargent by hemlock in both the overstory and understory. in the Pacific Northwest (Annand 1924), but it Hemlocks were heavily infested with adelgids and seldom injures forest hemlocks there (Keen 1938, showed injury in February 1986, even though trees Furniss & Carolin 1977). Annand (1928) and Carter had been infested for less than one year. The other (1971) believe that an adelgid collected from T. site was Gillette Castle State Park, which borders heterophylla and identified by Chrystal (1922) as East Haddam, Middlesex County, and Hadlyme, Chermes funitectus Dreyfus was also A. tsugae, New London County. Hemlocks were predomi- although no direct comparison of specimens was nant in the natural and cultivated areas of the park made. and were heavily infested with A. tsugae when this Despite the presence of A. tsugae in the United study was initiated. States for several decades and its importance as a Five hemlocks at each site were sampled by re- pest of T. canadensis in the East, very little has moving branches from the crown at the four car- been published on its biology and life cycle. Until dinal directions using a pole pruner. Samples were now, A. tsugae was thought to have a simple mono- collected weekly or biweekly from March through morphic life cycle represented by the partheno- November and monthly from December through genetic sistens which are restricted to hemlock. February for 2 yr. Sampled branches were exam- Host plants other than hemlock and winged and ined with a dissecting microscope, and the first 100 sexual stages of this adelgid were unknown (An- living individuals encountered on the most recent nand 1924, 1928). Here I report the results of stud- growth were mounted in Hoyer's medium on mi- ies conducted in Connecticut which revealed a croscope slides for detailed examination with a phase complex polymorphic life cycle of A. tsugae, and contrast light microscope. The number of exuviae

0013-8746/89/0050-0054$02.00/0 © 1989 Entomological Society of America January 1989 MCCLURE: POLYMORPHIC LIFE CYCLE OF Adelges tsugae 51

on hemlock, represented by the sistens present from July through April, and by the progrediens present from April through June (Fig. 2). The sistens ma- tured in February, and from March through May each of them produced a single white cottony ovi- sac containing 48.6 ±5.8 eggs. Between 40 and 50% of these eggs became progrediens, and the remainder became a migratory parthenogenetic generation, the sexupara. Nymphs of both types began hatching in April, quickly developed through four instars, and matured in June. Progrediens adults remained on hemlock, and during June and July

they produced cottony ovisacs similar to (but small- Downloaded from https://academic.oup.com/aesa/article/82/1/50/16507 by guest on 29 September 2021 er than) those produced by the sistens. These ovi- sacs contained 21.7 ± 3.6 eggs each. The sistens crawlers, which hatched from these eggs within a few days, settled on young hemlock branches, be- gan to feed, and soon thereafter entered an aesti- vation period that lasted several months. In Oc- tober, aestivating nymphs resumed development and matured by early February. The winged sex- Fig. 1. Distribution of hemlock woolly adelgid in upara adults that matured on hemlock in June mi- the eastern United States. grated to spruce, and in July each laid its comple- ment of 11.5 ± 3.6 eggs beneath its folded wings. associated with each specimen was counted to de- Adult sexupara produced eggs only on Picea species; termine the developmental instar; the exuviae from those that did not migrate to spruce died on hem- earlier moults usually remain among the woolly lock without producing eggs. The progeny of sex- secretion of each individual adelgid. Some speci- upara produced on spruce represented the sexual mens from each branch were cleared overnight in generation of A. tsugae called the sexuales. All the a 10% solution of KOH to enhance morphological sexuales nymphs that hatched and began to feed detail; other specimens were mounted uncleared on spruce in July died within a few days; none so that accurate measurements could be made. developed beyond the first instar on any of 12 Measurements were taken on a minimum of 100 different Picea species (McClure 1987). Therefore, specimens of each developmental stage per gen- the portion of the life cycle of A. tsugae that occurs eration and are reported here as means ± SD. on spruce remains a mystery. Drawings were made for each developmental stage Stages of Development. The oblong, amber-col- and were composites based upon examination of ored eggs of A. tsugae measured 0.36 ± 0.04 mm 100 specimens. long by 0.23 ± 0.03 mm wide for sistens and 0.35 On each sampling date, 1 kg of branches col- ± 0.04 mm long by 0.21 ± 0.03 mm wide for lected from each site was placed in emergence progrediens and sexupara. Eggs of the latter two cages (McClure 1977) so that any winged adelgids generations were produced simultaneously by the could be collected; these cages were maintained adult female sistens in what appeared to be a ho- until the following sampling date. The first 100 mogeneous cluster. Therefore, eggs of these two winged adelgids collected during each period were types could not be distinguished from one another. mounted and examined as described previously. Eggs of sexuales produced by the sexupara on spruce Fecundity of sistens and progrediens was deter- measured 0.37 ± 0.05 mm long by 0.25 ± 0.04 mined by counting the number of eggs and cho- mm wide. rions from hatched eggs within each of 10 ovisacs After hatching, the nymphs of all three gener- per branch (n = 100) in April and June, respec- ations of A. tsugae on hemlock developed through tively. Only ovisacs with dead adult females along- four instars before reaching maturity (Fig. 3 and side were examined to ensure that oviposition had 4), which is one more developmental instar than been completed. Fecundity of sexupara was de- adelgids were thought to have (Annand 1928). The termined in July by counting the number of eggs existence of this additional instar in A. tsugae and beneath the folded wings of 20 dead females col- in at least two other adelgid species, Pineus boer- lected from spruce species (McClure 1987). Vouch- neri Annand and P. coloradensis (Gillette), was er specimens have been deposited at the Connect- evident by the presence of four distinct nymphal icut Agricultural Experiment Station, Windsor. exuviae alongside individual adults for hundreds of specimens examined during this and an earlier investigation (McClure 1984). Throughout devel- Results opment, nymphs of sistens and progrediens were Life Cycle. During both years, A. tsugae com- very similar in size and appearance and could not pleted two wingless parthenogenetic generations be distinguished from one another reliably by mor- 52 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 82, no. 1

SPRUCE HEMLOCK

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Fig. 2. Polymorphic life cycle of A. tsugae alter- nating between hemlock and spruce.

phological features. Upon hatching, the crawlers (mobile first-instar nymphs) of A. tsugae were 0.44 ± 0.05 mm long by 0.27 ± 0.03 mm wide. Once they had settled, inserted their stylets, and begun to feed, these nymphs became much more heavily sclerotized and convex (Fig. 3B-E). Nymphs of sistens and progrediens also became disproportion- ately wide during the second, third, and fourth instars such that at maturity their legs did not ex- tend beyond the lateral margins of the thorax (Fig. 3F). The lengths and widths of these settled nymphs were as follows: first instar, 0.43 ± 0.04 mm long by 0.27 ± 0.03 mm wide; second instar, 0.57 ± Fig. 3. Life stages of sistens and progrediens of A. 0.05 mm long by 0.34 ± 0.04 mm wide; third instar, tsugae. (A) First-instar crawler. (B, C, D, E). Settled 0.67 ± 0.06 mm long by 0.43 ± 0.04 mm wide; first-, second-, third-, and fourth-instar nymphs, respec- fourth instar, 0.74 ± 0.06 mm long by 0.47 ± 0.05 tively. (F) Adult. mm wide. The antennae of first through fourth instars of sistens were similar in appearance to the antennae of first through fourth instars of progre- 0.35 ± 0.04 mm wide; third instar, 0.77 ± 0.07 diens (Fig. 5A, F-H). However, the antennae of mm long by 0.47 ± 0.05 mm wide; fourth instar, progrediens are somewhat longer and wider than 0.89 ± 0.09 mm long by 0.49 ± 0.05 mm wide. those of sistens throughout development, especially Enlargement of the thoracic areas in the third and during the second instar (Table 1). fourth instars of sexupara, related to the develop- The first-instar nymphs of sexupara and progre- ment of wings, provided an obvious means for dis- diens hatch simultaneously from eggs produced by tinguishing this generation of A. tsugae. In addition the same adult female sistens. Because hatching to their larger size, second-, third-, and fourth- nymphs appeared to be a homogeneous lot, pro- instar sexupara also differed from sistens and pro- grediens and sexupara could not be separated. Ac- grediens by having a distinguishing suture between cordingly, the drawings of the first-instar nymph the prothoracic and mesothoracic dorsal plate and of progrediens (Fig. 3B) and sexupara (Fig. 4A) a distinct wing bud notch along the posterior mar- are the same and represent a composite of the first gin of the mesothoracic dorsal plate (Fig. 4B-D). 100 specimens examined; presumably these in- The antennae of sexupara after the first instar also cluded both types. However, the remaining instars differed greatly from those of sistens and progre- of sexupara differed from those of sistens and pro- diens in shape and size (Fig. 5, Table 1). grediens in size, shape, and morphology, especially Adults of sistens and progrediens were readily with regard to thoracic and antennal structures distinguished from one another by their body size (Fig. 3-5). Sexupara nymphs were somewhat larger and by the relative lengths of their antennal seg- than those of sistens and progrediens and measured ments. Sistens adults measured 1.41 ± 0.17 mm as follows: second instar, 0.60 ± 0.07 mm long by long by 1.05 ± 0.12 mm wide, nearly twice as large January 1989 MCCLURE: POLYMORPHIC LIFE CYCLE OF Adelges tsugae 53

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Fig. 5. Antennae of A. tsugae. (A) First-instar nymph of all generations. (B, C) Second- and third-instar nymphs, respectively, of sexupara. (D) Fourth-instar pupa of sex- Fig. 4. Life stages of sexupara of A. tsugae. (A) upara. (E) Adult sexupara. (F, G, H) Second-, third-, and Settled first-instar nymph (indistinguishable from that of fourth-instar nymph, respectively, of sistens and progre- progrediens, Fig. 3B, see text). (B, C) Settled second- diens. (I) Adult sistens. (J) Adult progrediens. and third-instar nymphs, respectively. (D) fourth-instar pupa. (E) Adult. (F) Adult wings. The winged adult sexupara measured 1.09 ± 0.10 mm long by 0.51 ± 0.06 mm wide and were as progrediens adults, which measured 0.87 ± 0.09 dark brown and heavily sclerotized (Fig. 4). Their mm long by 0.63 ± 0.07 mm wide. Adult sistens long five-segmented antennae (Table 1; Fig. 4) to- also were more heavily sclerotized than adult pro- gether with the presence of compound eyes and grediens and had many more wax-producing glands four textured wings (Fig. 4) readily distinguished distributed throughout the dorsum. The length of them from adult sistens and progrediens. the terminal antennal segment of an adult sistens was subequal to the length of the two basal seg- ments combined, whereas the length of the ter- Discussion minal segment of an adult progrediens was nearly Adelges tsugae has several more life forms and twice the length of the combined basal segments has a much more complex life cycle than had been (Fig. 5). reported previously. In addition to two wingless

Table 1. Length and width of the antennae of the life stages of A. tsugae on hemlock

Generation Stage Sistens Progrediens Sexupara Length Width Length Width Length Width Nymph I 95.8 ± 9.8 24.2 ± 3.1 98.6 ± 10.1 25.4 ± 3.1 98.6 ± 9.9 25.4 ± 3.1 Nymph II 67.9 ± 7.1 23.6 ± 2.4 90.2 ± 9.7 28.8 ± 2.5 101.7 ± 10.7 31.3 ± 3.3 Nymph III 64.2 ± 6.9 25.1 ± 3.4 64.8 ± 7.1 28.6 ± 3.0 116.9 ± 12.1 39.4 ± 4.1 Nymph IV 60.8 ± 6.9 25.4 ± 2.9 61.9 ± 6.9 28.6 ± 3.2 169.3 ± 15.7 44.6 ± 4.7 Adult 61.1 ±7.3 28.5 ± 3.9 67.0 ± 7.7 28.8 ± 3.1 240.6 ± 23.6 39.1 ± 3.9

All measurements are means (in microns) ± SD; n > 100. 54 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 82, no. 1 parthenogenetic generations which remain on erations, its high reproductive potential, and the hemlock, there is a third migratory, parthenoge- lack of any other significant mortality factors. As netic generation, the sexupara, which matures as A. tsugae continues to spread, it may eventually winged adults, a life stage previously unknown for encounter a spruce species, probably an exotic one this insect. For all known adelgids, the develop- in cultivation, on which it can survive and repro- ment of winged adults on a host species other than duce. Most likely this would be the same or a similar spruce is indicative of a migratory life cycle which Picea species on which A. tsugae evolved in its alternates between Picea and one of several other homeland. Should this happen, the threat to hem- genera of including Abies, Larix, Pinus, lock could be enhanced because generations of A. Pseudotsuga, and Tsuga (Annand 1928, Carter tsugae developing on spruce could migrate back 1971). Some adelgids never produce winged forms to hemlock and contribute significantly to the spread and never alternate between primary and inter- and growth of adelgid populations on this host. mediate hosts. However, the fact that A. tsugae Downloaded from https://academic.oup.com/aesa/article/82/1/50/16507 by guest on 29 September 2021 did produce winged sexupara on hemlock estab- Acknowledgment lished an important link with spruce. Previous experiments in the laboratory and in I am grateful to B. R. Beebe for her drawings of the field revealed that adult sexupara migrated to adelgid life stages and for her technical assistance during and laid eggs of sexuales on 12 different spruce this investigation. I thank the Connecticut Nature Con- species (McClure 1987). The Picea species tested servancy and Gillette Castle State Park for allowing me that are native to North America were P. engel- to conduct studies on their properties. mannii (Parry), P. glauca (Moench) Voss, P. mari- ana (Mill.) Britton, P. pungens Engelmann, P. ru- References Cited bens Sargent, and P. sitchensis (Bong.) Carriere. Annand, P. IS. 1924. A new species of Adelges (He- The exotic tested included P. abies (L.) miptera, Phylloxeridae). Pan-Pac. Entomol. 1: 79-82. Karsten from Europe and P. asperata Masters, P. 1928. A contribution toward a monograph of the heterolepis Rheder and Wilson, P. jezoensis (Sieb. Adelginae (Phylloxeridae) of North America. Stan- and Zucc.) Carriere, P. orientalis (L.) Link. Car- ford University, Palo Alto, Calif. riere, and P. polita Carriere from Asia. However, Carter, C. I. 1971. woolly aphids (Adelgidae) none of the sexuales nymphs that hatched and fed in Britain. Bull. For. Comm. Lond. 42. upon these spruces lived for more than a few days. Chrystal, R. N. 1922. The Douglas fir chermes None developed beyond the first instar. Because (Chermes cooleyi). Bull. For. Comm. Lond. 4. these sexuales had inserted their stylets into the Furniss, R. L. & V. M. Carolin. 1977. Western forest 4 plant and had begun to feed, it does not appear . USDA Miscellaneous Publication 1339. that any of the 12 Picea species tested is a suitable Keen, F. P. 1938. Insect enemies of western forests. USDA Miscellaneous Publication 273. host for A. tsugae (McClure 1987). All of the rel- McClure, M. S. 1977. Parasitism of the scale insect, atively few sexupara that did not leave hemlock Fiorinia externa (Homoptera: Diaspididae) by As- died without laying eggs and, therefore, did not pidiotiphagus citrinus (Hymenoptera: Eulophidae) contribute individuals to the population on that in a hemlock forest: density dependence. Environ. host (McClure 1987). Entomol. 6: 551-555. The apparent lack of a suitable spruce species 1984. Influence of cohabitation and resinosis on site for A. tsugae in the northeastern United States selection and survival of Pineus boerneri Annand and resulted in a substantial loss of individuals to the P. coloradensis (Gillette) (Homoptera: Adelgidae) on red pine. Environ. Entomol. 13: 657-663. population on hemlock each year. During 1986 and 1987. Biology and control of hemlock woolly adelgid. 1987, more than half of the offspring produced by Bulletin of the Connecticut Agricultural Experiment the sistens developed into winged sexupara, which Station 851. left hemlock in an unsuccessful attempt to locate Takahashi, R. 1937. Phylloxeridae of Formosa (He- a suitable spruce species. However, despite this miptera). Trans. Nat. Hist. Soc. Formosa 27: 11-14. significant loss of individuals to the population each year, A. tsugae was still able to increase its numbers Received for publication 11 February 1988; accepted rapidly on hemlock because of its two annual gen- 9 August 1988.