Two Teams with a New Take: Insect Losses Due to Invasive Plants

I have been impressed recently by two groups of scientists who are trying to broaden understanding of the impacts of invasive plants by examining the interactions of those plants with insects. As they note, herbivorous insects are key players in terrestrial food webs; they transfer energy captured by plants through photosynthesis to other trophic levels. This importance has been recognized since Elton first established the basic premises of food webs (1927) [Burghardt et al.; full citation at end of blog] Arthropods comprise significant members of nearly every trophic level and are especially important as pollinators. If introduced plants cause changes to herbivore communities, there will probably be effects on predators, parasites, and other wildlife through multitrophic interactions [Lalk et al.; Tallamy, Narango and Mitchell].

[I briefly summarize the findings of a third group of scientists at the end of this blog. The third group looks at the interaction between agriculture – that is, planting of non-native plants! – and climate change.]

One approach to studying this issue, taken by Douglas Tallamy of the University of Delaware and colleagues, is to look at the response of herbivorous insects to NIS woody plants fairly generally. They integrate their studies with growing concern about the global decline in insect populations and diversity. They note that scientists have focused on light pollution, development, industrial agriculture, and pesticides as causes of these declines. They decry the lack of attention to disruption of specialized evolutionary relationships between insect herbivores and their native host plants due to widespread domination by non-indigenous plants [Richard, Tallamy and Mitchell].

In their studies, Tallamy and colleagues consider not just invasive plants, but also non-native plants deliberately planted as crops or ornamentals, or in forestry. They point out that such introduced plants have completely transformed the composition of plant communities in both natural and human-dominated ecosystems around the globe. At least 25% of the world’s planted forests are composed of tree species not native to their locale. At least one-sixth of the globe is highly vulnerable to plant invasions, including biodiversity hotspots [Richard, Tallamy and Mitchell].

A different approach, taken by Lalk and colleagues, is more closely linked to concern about impacts of the plants themselves. They have chosen to pursue knowledge about relationships between individual species of invasive woody plants and the full range of arthropod feeding guilds – pollinators, herbivores, twig and stem borers, leaf litter and soil organisms. In so doing, they decry the general absence of data.

Both teams agree that:

• Invasive plants are altering ecosystems across broad swaths of North America and the impacts are insufficiently understood.
• The invasive plant problem will get worse because non-native species continue to be imported and planted. (Reminder: the Tallamy team considers impacts of deliberate planting as well as bioinvasion.)
• Plant-insect interactions are the foundation of food webs, so changes to them will have repercussions throughout ecosystems.

Tallamy team

Non-native plants have replaced native plant communities to a greater or lesser extent in every North American biome – including anthropogenic landscapes [Burghardt]. The first trophic level in suburban and urban ecosystems throughout the U.S. is dominated by plant species that evolved in Southeast Asia, Europe, and South America [Tallamy and Shropshire]. Abundant non-native plants not only dominate plant biomass; they also reduce native plant taxonomic, functional and phylogenetic diversity and heterogeneity. Thus, they indirectly alter the abundance of native insects  [Burghardt; Richard, Tallamy and Mitchell].

I think these articles might actually underestimate the extent of these impacts. While Richard, Tallamy and Mitchell report that more than 3,300 species of non-native plants are established in continental U.S., years ago Rod Randall said that more than 9,700 non-native plant species were naturalized in the U.S. (probably includes Hawai` i.   The Tallamy team cites USDA Forest Service data showing 9% of forests in the southeast are invaded by just 33 common invasive plant species [Richard, Tallamy and Mitchell], I have cited that and other sources showing even greater extents of plant invasion in the east and here; other regions and here. 

The Tallamy team has conducted several field experiments that demonstrate that the presence of non-native plants suppress numbers and diversity of native lepidopteran caterpillars. These non-native woody plants have not replaced the ecological functions of the native plants that used to support insect populations. This is true whether or not the non-native plants are deliberately planted or are invading various ecosystems on their own. [Richard, Tallamy and Mitchell]. (Of course, they expect plant invasions to grow; they note that some of the many ornamental species that are not yet invasive will become so.)

The result is disruption of the ecological services delivered by native plant communities, including the focus of their studies: plants’ most fundamental contribution to ecosystem function: generation of food for other organisms [Burghardt].

They note that plants’ relationship to insects differs depending on the insects’ feeding guilds — folivores, wood eaters, detritivores, pollinators, frugivores, and seed-eaters; and among herbivores with different mouthparts — chewing or sucking; and as host plant specialists or generalists. They decry studies that fail to recognize these differences [Tallamy, Narango, and Mitchell].

The Tallamy team explores why insect populations decline among non-native plants. That is,  

1) Do insects directly requiring plant resources have lower fitness when using non-native plants; do they not recognize them as viable host plants; or do they avoid them altogether? 

2) Are reductions in numbers of specialist herbivores mitigated by generalists? A decade of research shows that both specialists and generalists decline.

The team’s studies focus on lepidopteran larvae (caterpillars). Insect herbivores are both the largest taxon of primary consumers and extremely important in transferring energy captured by plants through photosynthesis to other trophic levels [Burghardt]. In addition, insects with chewing mouthparts are typically more susceptible to defensive secondary metabolites contained in leaves than are insects with sucking mouthparts that tap into poorly defended xylem or phloem fluids [Tallamy, Narango and Mitchell].

A study by Burghardt et al. found that 75% of all lepidopteran species and 93% of specialist species were found exclusively on native plant species. Non-native plants that were in the same genus as a native plant often supports a lepidopteran community that is a similar but depauperate subset of the community found on its native congener. In fact, the insect abundance and species richness supported by non-native congeners of native species was reduced by 68%.

A meta-analysis of 76 studies by other scientists found that, with few exceptions, caterpillars had higher survival and were larger when reared on native host plants. Plant communities invaded by non-native species had significantly fewer Lepidoptera and less species richness. In three of eight cases examined, non-native plants functioned as ecological traps, inducing females to lay eggs on plants that did not support successful larval development. Richard, Tallamy and Mitchell cite as an example the target of many conservation efforts, monarch butterflies (Danaus plexxipus), which fail to reproduce when they use nonnative swallowworts (Vincetoxicum species.) instead of related milkweeds (Asclepias species.).

Tallamy and Shropshire ranked 1,385 plant genera that occur in the mid-Atlantic region by their ability to support lepidopteran species richness. They found that introduced ornamentals are not the ecological equivalents of native ornamentals. This means that solar energy harnessed by introduced plants is largely unavailable to native specialist insect herbivores.

Tallamy, Narango, and Mitchell describe the following patterns:

1) Insects with chewing mouthparts are typically more susceptible to defensive secondary metabolites contained in leaves than are insects with sucking mouthparts that tap into poorly defended xylem or phloem fluids. As a result, sucking insects find novel non-indigenous plants to be acceptable hosts more often. However, there are more than 4.5 times as many chewing (mandibulate) insect herbivores than sucking (haustellate) species. It follows that the largest guild of insect herbivores is also the most vulnerable to non-native plants as well as being the most valuable to insectivores.

2) Woody native species, on average, support more species of phytophagous insects than herbaceous species.

3) Although insects are more likely to accept non-native congeners or con-familial species as novel hosts, non-native congeners still reduced insect abundance and species richness by 68%.

4) Host plant specialists are less likely to develop on evolutionarily novel non-indigenous plants than are insects with a broader diet. There are far more specialist species than generalists, so generalists will not prevent serious declines in species richness and abundance when native plants are replaced by non-indigenous plants. In addition, non-native plants cause significant reductions in species richness and abundance even of generalists. In fact, generalists are often locally specialized on particular plant lineages and thus may function more like specialists than expected.

5) Any reduction in the abundance and diversity of insect herbivores will probably cause a concomitant reduction in the insect predators and parasitoids of those herbivores – although few studies have attempted to measure this impact beyond spiders, which are abundant generalists. The vast majority of parasitoids are highly specialized on particular host lineages.

6) Studies comparing native to non-native plants must avoid using native species that support very few phytophagous insects as their baseline, e.g., in the mid-Atlantic region tulip poplar trees (Liriodendron tulipifera) and Yellowwood (Cladrastus kentuckea).

7) Insects that feed on well-defended living tissues such as leaves, buds, and seeds are less likely to be able to include non-native plants in their diets than are insects that develop on undefended tissues like wood, fruits, and nectar. Although this hypothesis has never been formally tested, they note the ease with which introduced wood borers – emerald ash borer, Asian longhorned beetle, polyphagous and Kuroshio shot-hole borers, redbay ambrosia beetle, Sirex woodwasp (all described in profiles posted here — have become established in the US.

Lalk and Colleagues

As noted, Lalk and colleagues have a different frame; they focus on individual introduced plant species rather than starting from insects. They also limit their study to invasive plants. The authors say there is considerable knowledge about interactions between invasive herbaceous plants and arthropod communities, but less re: complex interactions between invasive woody plants and arthropod communities, including mutualists (e.g., pollinators), herbivores, twig- and stem-borers, leaf-litter and soil-dwelling arthropods, and other arthropod groups.

They ask why this knowledge gap persists when invasive shrubs and trees are so widespread and causing considerable ecological damage. They suggest the answer is that woody invaders rarely encroach on high-value agricultural systems and some are perceived as contributing ecosystem services, including supporting some pollinators and wildlife.

Lalk and colleagues seek to jump-start additional research by summarizing what is currently known about invasive woody plants’ interactions with insects. They found sufficient data about 11 species – although even these data are minimal. They note that all have been cultivated and sold in the U.S. for more than 100 years. All but one (mimosa) are listed as a noxious weed by at least one state; two states (Rhode Island and Georgia) don’t have a noxious weed list. None of the 11 is listed under the federal noxious weed statute.

Illustrations of how minimal the existing information is:

• Tree-of-heaven (Ailanthus altissima) is noted to be supporting expanded populations of the Ailanthus webworm moth (Atteva aurea), which is native to Central America; and to be the principal reproductive host for SLF (Lycorma delicatua)  https://www.dontmovefirewood.org/pest_pathogen/spotted-lanternfly-html/
• Chinese tallow (Triadica sebifera) is thought to benefit both native generalist bee species and non-indigenous European honeybees (Apis mellifera).
• Chinese privet (Ligustrum sinense) appears to suppress populations of butterflies, bees, and beetles.

Lalk and colleagues then review what is known about interactions between individual invasive plant species in various feeding guilds. They point out that existing data on these relationships are scarce and sometimes contradictory.

They believe this is because interactions vary depending on phylogenetic relationships, trophic guild, and behavior (e.g., specialized v. generalist pollinator). Arthropods can be “passengers” of a plant invasion. That is, they can be affected by that invasion, with follow-on effects to other arthropods in the community. Also, arthropods can be “drivers” of invasion, increasing the success of the invasive plants.

They then summarize the available information on various interactions. For example, they note that introduced plants can compete with native plants in attracting pollinators, causing cascading effects. Or they can increase pollination services to native plants by attracting additional pollinators.

They note that herbivore pressure on invasive plants can have important impacts on growth, spread, and placement within food webs. They note that these cases support the “enemy release hypothesis”, although they think there are probably additional driving mechanisms.

Lalk and colleagues note that most native twig- and stem-borers (Coleoptera: Buprestidae, Curculionidae, Cerambycidae; Hymenoptera: Siricidae) are not considered primary pests but that some of our most damaging insect species are wood borers (see above).

Some of these borers are decomposers; in that role, they are critical in nutrient cycling.

Arthropods in leaf litter and soil also serve important roles in the decomposition and cycling of nutrients, which affects soil biota, pH, soil nutrients, and soil moisture. They act as a trophic base in many ecosystems. Lalk and colleagues suggest these arthropod communities probably change with plant species due to differences in leaf phytochemistry. They cite one study that found litter community composition differed significantly between litter beneath tree-of-heaven, honeysuckle (Lonicera maackii), and buckthorn (Rhamnus cathartica) compared to litter underneath surrounding native trees.

Recommendations

Both the Tallamy and Lalk teams call for ending widespread planting of non-native plants. Lalk and colleagues discuss briefly the roles of

• The nursery industry (including retailers); they produce what sells.
• Scientists and educators have not sufficiently informed home and land owners about which species are invasive or about native alternatives.
• Private citizens buy and plant what their neighbors have, what they consider aesthetically pleasing, or what is being promoted.
• States have not prohibited sale of most invasive woody plants. Regulatory actions are not a straightforward matter; they require considerable time, supporting information, and compromise.

Tallamy team calls for restoration ecologists in the eastern U.S. to consider the number of Lepidopterans hosted by a plant species when deciding what to plant. For example, oaks (Quercus), willows (Salix), native cherries (Prunus)and birches (Betula) host orders of magnitude more lepidopteran species in the mid-Atlantic region than tulip poplar.(Those lepidopteran in turn support breeding birds and other insectivorous organisms.) [Tallamy & Shropshire]

Lalk and colleagues focused on identifying several key knowledge gaps:

• How invasive woody plants affect biodiversity and ecosystem functioning
• How they themselves function in different habitats.
• Do non-native plants drive shifts in insect community composition, and if so, what is that shift, and how does it affect other trophic levels?
• How do IAS woody plants affect pollinators?

The authors do not minimize the difficulty of separating such possible plant impacts from other factors, including climate change and urbanization.

Global Perspective

Outhwaite et al. (full citation at end of this blog) note that past studies have shown that insect biodiversity changes are driven primarily by land-use change (which is another way of saying planting of non-native species – as Dr. Tallamy and colleagues describe it) and increasingly by climate change. They south to examine whether these drivers interact. They found that the combination of climate warming and intensive agriculture is associated with reductions of almost 50% in the abundance and 27% in the number of species within insect assemblages relative to levels in less-disturbed habitats with lower rates of historical climate warming. These patterns were particularly clear in the tropics (perhaps partially because of the longer history of intensive agriculture in temperate zones). They found that high availability of nearby natural habitat (that is, native plants) can mitigate these reductions — but only in low-intensity agricultural systems.

Outhwaite et al. reiterate the importance of insect species in ecosystem functioning, citing pollination, pest control, soil quality regulation & decomposition. To prevent loss of these important ecosystem services, they call for strong efforts to mitigate climate change and implementation of land-management strategies that increase the availability of natural habitats.

SOURCES

Burghardt, K. T., D. W. Tallamy, C. Philips, and K. J. Shropshire. 2010. Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere 1(5):art11. doi:10.1890/ES10-00032.

Lalk, S. J. Hartshorn, and D.R. Coyle. 2021. IAS Woody Plants and Their Effects on Arthropods in the US: Challenges and Opportunities. Annals of the Entomological Society of America, 114(2), 2021, 192–205 doi: 10.1093/aesa/saaa054

Outhwaite, C.L., P. McCann, and T. Newbold. 2022.  Agriculture and climate change are shaping insect biodiversity worldwide. Nature 605 97-192 (2022)  https://www.nature.com/articles/s41586-022-04644-x

Richard, M. D.W. Tallamy and A.B. Mitchell. 2019. Introduced plants reduce species interactions. Biol Invasions

Tallamy, D.W., D.L. Narango and A.B. Mitchell. 2020. Ecological Entomology (2020), DOI: 10.1111/een.12973 Do Non-native plants contribute to insect declines?

Tallamy, D.W. and K.J. Shropshire. 2009. Ranking Lepidopteran Use of Native Versus Introduced Plants Conservation Biology, Volume 23, No. 4, 941–947 2009 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2009.01202.x

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm