Ron Wilson

Ron Wilson

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The Fascinating Complex Life Cycle of Hemlock Wooly Adelgid

The Ohio State University, C. Wayne Ellett Plant Pest Diagnostic Clinic (CWE-PPDC) received a sample of eastern hemlock (Tsuga canadensis) that was infested with hemlock woolly adelgid from Hocking State Forest, Ohio in September 2024.

 

One of the affected hemlock trees (left) Image © Mikayla Heydt, Regional Forest Health Coordinator, Hocking State Forest, and a twig showing HWA with the characteristic white woolly masses (right). See Image

  

Hocking county, where Hocking State Forest is located, is already in quarantine for HWA to prevent its movement from infested to uninfested counties in Ohio. We informed the park authorities of our finding and requested they report the incident to the Ohio Department of Agriculture (ODA), using the reporting tool.

 

On the hemlock sample submitted, we observed the cottony masses covering HWA adults (right), crawlers (left), and overwintering nymphs (below link). These cotton masses probably protect the female insect and their eggs from predators and desiccation. The feeding location by the adelgids is usually restricted to the base of the hemlock needles (below link).

 

The overwintering generation of HWA settles on the base of the needles during early summer and undergoes a diapause from late summer until late fall. This diapause period is thought to allow them to avoid developing at a time when the trees offer less nutrition, and to set up the timing of the spring generation. During the winter, they are mostly dormant but can start feeding as the weather warms and develop into adult females by late winter to early spring.

  

After looking into the timing of HWA development, I became fascinated by the complex life cycle of HWA and how they have managed to thrive in the United States. The more I read, the more interesting the story became, generating lots of questions. The aim of this article is to break down the complex life cycle of HWA in a way that's accessible to readers with the help of experts, Kayla I. Perry, OSU forest entomologist and Nathen P. Havill, Research Entomologist, USDA Forest Service, providing key insights into their survival and spread.

  

The best way to start the story is from an incident reported in the Portsmouth Herald link in New Hampshire and other news outlets in early June 2021. Reports included images that showed York County beaches in southern Maine covered by a black substance that stained the feet of beach visitors, and that the stain did not come off with soap and water.

 

People that visited beaches in southern Maine on June 7, 2021, reported in Portsmouth Herald, NH.

  

Similar reports from other beaches in southern New England surfaced with concerns that this substance may be hazardous. During a separate incident, a boater near a beach in Beverly, Massachusetts reported trillions of tiny dead insects falling from the sky and littering his boat (Havill et al., 2022). From the images provided by the public and after collecting a sample from Wells Beach in southern Maine, the Maine Department of Agriculture, Conservation and Forestry (DACF) concluded that those tiny black particles were countless insects that had deposited on the shore when the tide receded.

 

Nathan Havill and his team at the USDA Forest Service, later identified these insects with morphological and molecular methods, as the winged form of HWA.  It turned out that massive numbers of this invasive species had been blown out to sea during the point in its life cycle when winged migrants are produced,and had washed up on the beaches.

  

Taxonomy and Identification

HWA is a hemipteran insect in the family Adelgidae. There are two adelgid genera, Adelges and Pineus, both of which are reported in North America.

 

Thirty-seven species of Adelges are reported globally, with twelve species found in North America. While adelgids share common characteristics with aphids (Aphididae) and phylloxerns (Phylloxeridae), but they diverged from these groups millions of years ago and have some interesting distinctions. Unlike aphids, adelgids and phylloxerans do not have cornicles (appendages on the end of the abdomen that secrete pheromones and defensive chemicals), and they lay eggs in all generations, unlike aphids which can give birth to live young. Phylloxerans and many aphids feed on angiosperms, but adelgids feed only on certain conifer genera in the Pinaceae (Havill & Foottit 2007).

 

There are at least 9 distinct genetic lineages of HWA endemic to different regions in the world: two each in China, Taiwan, and Japan and one each in Ulleung Island, South Korea and western North America (Havill et al. 2016). Recently, a new lineage was also found in Bhutan (N.P. Havill, unpublished). It is estimated that the different adelgid lineages began to diversify around 30 million years ago (Havill et al. 2007), during a time period closely aligned with the evolutionary diversification of Tsuga species. The different lineages of HWA are genetically and behaviorally diverse, and some of them will likely be described as separate species. The lineage that invaded eastern North America came from southern Japan where it feeds on southern Japanese hemlock, Tsuga sieboldii, and tigertail spruce, Picea polita. In contrast, HWA in western North America was surprisingly found to be native to that region, not introduced, as was previously thought, so this region has been a focus of the search for biological control agents that co-evolved with HWA (Mayfield et al. 2023).

 

HWA eggs and crawlers (left) image © Michael Montgomery, USDA Forest Service, Bugwood.org, and HWA crawler (right), image © Kelly Oten, North Carolina State University, Bugwood.org

  

When was HWA first reported in North America, and what is being done about it?  

Native to Asia, HWA was first reported in the eastern United States with specimens deposited at the U.S. National Insect Collection that were collected in Richmond, Virginia, in 1951. It is possible that it was introduced on ornamental trees imported from Japan at a time when planting Japanese style gardens was very popular. HWA first spread very slowly, but once it reached areas of higher hemlock abundance, it spread very rapidly to encompass more than half of the range of eastern hemlock, as it continues to spread north and west. Eastern hemlock species have little resistance to HWA, and native predators are not effective at regulating the populations. Management strategies include the release of biological control agents from its native ranges, and chemical treatments, yet the adelgid continues to pose a major threat to forest ecosystems and biodiversity.

 

This ODNR article provides information about HWA in Ohio with the reporting tool, including current counties that are in quarantine in Ohio.

 

Thomas deHass and Ann Chanon published this article with control options for HWA in this 2023 BYGL article.

  

HWA life cycle in its native ranges

 

The full life cycle (holocycle) of HWA in its native ranges in Asia takes two years to complete and requires both hemlock and spruce. Sexual reproduction only occurs in the generation just before gall-making on spruce. All of the other generations on spruce and hemlock are asexual. A proportion of the second generation on hemlock can stay on hemlock, so if no spruce hosts that it can survive on are available to complete the holocycle, then continuous asexual generations can keep reproducing on hemlock (anholocycle). ImageVince D’Amico and Nathan Havill, 2016.

  

The formation of galls on spruce is an integral feature of the adelgid holocycle. The galls are formed as a result of adelgid feeding, and they provide a nutritious and safe environment for adelgid development. HWA uses different spruce species in different regions. It uses Picea polita in Japan, Picea likiangensis and Picea brachytyla in China, Picea morrisonicola in Taiwan, and Picea spinulosa in Bhutan. It is not known whether the different adelgid lineages in these different regions can use spruce species native to other regions. The galls on Picea polita in Japan can grow up to 4 cm in diameter and can house more than 1000 adelgids. When the galls mature and begin to dry out, winged adelgids called gallicolae, about 2 mm in length, emerge to fly to hemlock hosts. After landing on hemlock, the winged adelgids lay eggs that hatch and the mobile first instar crawlers move to settle at the base of needles and then overwinter, joining the generation of wingless individuals at the base of the needles that stayed on hemlock. The crawlers insert their long stylets into the xylem to begin feeding on nutrients inside the living parenchyma cells (see below image). After overwintering, this generation of entirely wigless females, called sistens, develop to the adult stage and begin laying eggs in late winter to early spring. These eggs begin to hatch in mid spring, and again settle at the base of the needles. In this next generation, a proportion develop to be wingless adults, called progrediens, and a proportion become winged adults, called sexuparae. The wingless progrediens give rise to more sistens, while the sexuparae fly to spruce where they land on the needled and give rise to sexual females and males. Each mated female has a single offspring, called the fundatrix, that crawls and settles at the base of a developing spruce bud, causing it to begin swelling into a gall. The fundatrix has a large number of gallicola offspring that crawl into the developing gall to begin the cycle again.

 

HWA gall on tiger-tail spruce, Picea polita, in Japan (left). An HWA nymph feeding at the base of a hemlock needle (middle). The white arrow shows the insertion point of its long stylet into the base of the needle to feed on nutrients in the xylem parenchymal cells. The insertion point and the stylet inside the plant (right). images © Havill et al., 2016 The left photo was taken by Shigehiko Shiyake, Osaka Museum of Natural History, and the other 2 by Kathleen Shields, USDA Forest Service.

 

HWA life cycle in the introduced range

In eastern North America, HWA unfortunately thrives on eastern and Carolina hemlocks causing it to be a devastating pest. But perhaps fortunately, it cannot survive on native spruce species. This results in a truncated, entirely anholocyclic life cycle with only the two asexual generations on hemlock. Genetic analysis has shown that there is remarkably only a single genetic clone throughout all of eastern North America, confirming that sexual reproduction is non-existent or very rare in its introduced range (Havill et al. 2016). The lack of sexual reproduction might slow it ability to adapt, but it still has enormous reproductive potential in the eastern United States, with each female producing up to 200 eggs.

 

Picea polita has not been planted widely as an ornamental in the United States, and but a handful of arboreta, botanical gardens, and college campuses have planted this species. Several of these have been examined for presence of HWA galls (e.g. Arnold Arboretum in Massachusetts, Maymont Park in Virginia, the Cornell University campus in New York), but they have not been found despite HWA being abundant in those places (N.P. Havill, unpublished). We do not know why these ornamental Picea polita are apparently not supporting the rest of the HWA holocycle in its introduced range.

 

Worldwide distribution of hemlock (Tsuga) species. Modified from Havill et al. (2008).

 

Hemlock species in North America and HWA

Havill et al. (2008) demonstrated that the two eastern North American hemlock species are not closely related. Tsuga canadensis diverged early in the genus' evolutionary history, while T. caroliniana diverged more recently and is more closely related to the Asian species. This relationship aligns with the ability of T. caroliniana to hybridize with Asian hemlocks that are resistant to HWA, whereas attempts to cross T. canadensis with these species have failed. Hybrids between T. caroliniana and T. chinensis, developed by the U.S. National Arboretum are resistant to HWA and could serve as viable replacements for T. canadensis in urban environments. T. chinensis itself is highly resistant to HWA and thrives in the northeast United States. Link

 

The two western North American species of hemlock, Tsuga heterophylla (western hemlock) and Tsuga mertensiana (mountain hemlock), are more resistant or tolerant to HWA compared to the eastern species. However, these western species do not survive well in the eastern United States (Havill et al., 2011).

  

The real question - why HWA can’t survive on North American spruce?

While different systems provide different classifications, there are currently ten species of spruce (Picea spp.) reported in North America by Weng & Jackson, 1999, with 7 of those being native species. Three species of Picea are documented to be native to eastern North America, P. rubens, P. mariana, and P. glauca. None of these, or any other North American spruce species, are hosts for HWA. This raises several questions, including why is HWA unable to use native North American spruce species as hosts to complete the sexual generation, and could it evolve to use these hosts in the future?

 

Distribution of Picea species in North America according to Weng & Jackson, 2000 (may not represent accurate statewide distribution of Picea species in the United States). Map compiled by Suranga Basnagala, OSU Entomology.

  

McClure (1987) link investigated the survival and reproductive potential of the invasive Japanese HWA lineage on 12 native and non-native species of spruce using a combination of field and laboratory experiments. He found that when winged females that emerged from hemlock (sexuparae) were placed on spruce, they successfully laid eggs. Those eggs hatched, and the first instar crawlers (sexuales) settled and began to feed on spruce but died within few days. None developed beyond the first instar on any of the 12 Picea species tested. This included Picea polita, which is now confirmed to be the primary host of HWA in Japan, which adds to the mystery of why only some trees in this species appear to be acceptable hosts.

 

Given our experiences with other forest insect invasions, we might expect native North American spruces to be susceptible to exotic HWA due to a lack of defenses because they do not share a recent coevolutionary history. But unlike eastern North American hemlocks, they are not. Recent work by a consortium of scientists found that native tree species that are too closely or too distantly related from an insects native hosts are less likely to be highly impacted by a non-native insect, than those at an intermediate evolutionary distance. It might be the case that eastern hemlocks fall into this unfortunate Goldilocks zone while eastern spruces do not.

 

While HWA does not need spruce to survive, there might be a possibility for them to adapt and continue their sexual generation on eastern spruces in the future. This is probably highly unlikely though, since host suitability is a very complex trait, and other processes might be working against it. Which brings us back to what people experienced in 2021 on southern New England beaches. It might have been a rare phenomenon when millions, if not trillions, of winged HWA washed up on the beaches like they did – the weather conditions might have been just right for that to happen that day. But the fact that so many HWA fly out to trying to find their primary spruce host, but fail and die in massive numbers highlights another, probably stronger selective pressure on HWA in its introduced range. The proportion of winged adelgids that each adelgid produces in the second generation on hemlock each year is inversely proportional to their fitness – more winged offspring equals lower fecundity. So, there is probably strong selection against producing them. It will be interesting to see if the proportion of sexuparae does indeed go down over time, and maybe after tens, or thousands, of years, there may not be any migrants left, making the suitability of eastern spruces a moot point.

 

Research can make predictions based on observations which becomes facts, but right now only HWA knows the underlying causes to this mystery. Perhaps it's time to think like HWA to uncover the answer!


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