Photo: Salt cedar & Giant Cane on the Rio Grande, Big Bend National Park. © 2017 Delena Norris-Tull
Indirect impacts of biocontrol insects on native species
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, July 2020, updated December 2024.
Boettner et al., 2000, examined the indirect non-target effects of the introduction of Compsilura concinnata (a parasitoid fly introduced into North America repeatedly from 1906 to 1986, for control of gypsy moths) on native moths, including a silk moth. They deployed, in the field, larvae of two native silk moth species to examine the attack rate by Compsilura concinnata. They found high levels of parasitism in all samples studied, up to 100% in some samples. They warned that indirect non-target effects could potentially be responsible for extinctions, at least locally, of native insect species.
They also found that few studies had been done on the ecological impact of this and other introduced invertebrates, including the Asian lady beetle (Harmonta axyridis), which was introduced for biological control in the eastern US and Canada over several decades into the 1990s, and is now abundant and widespread in the US and Canada. The Asian lady beetle is now considered one of the most invasive insects. This species has resulted in the decline of native ladybird species and some other insects."
Boettner et al., 2000, warned that, as of 2000, federal requirements and funding for testing the ecological impacts of biological control agents is inadequate.
Hennemann and Memmott, 2001, warned that looking solely at direct effects on non-target plant species is not adequate to determine ecological impacts of biocontrol agents. They found that, “Indirect effects on native [insect] species are the most difficult to assess. An insect herbivore introduced to control a weed could be attacked by generalist native parasitoids that also have native hosts. If the… biological control agent is abundant, then there is the potential for apparent competition between the agent and native [insect] herbivores, mediated via shared native parasitoids. Thus, even the introduction of an entirely species-specific herbivore, presumed to have no nontarget effects, still could have a community-wide impact. Only by understanding how invasive species interact within the context of the entire community can we hope to assess the risks to native species, whether they be direct effects on single species or indirect effects on several species across trophic levels.”
“There have been at least 122 releases of parasitic wasps and flies against agricultural pest Lepidoptera in Hawaii within the past 100 years, providing high potential for nontarget effects, particularly on leaf-feeding [native] caterpillars” (Hennemann & Memmott, 2001).
Hennemann and Memmott, 2001, conducted an extensive field study of parasitoids found in moths in the remote Alakai Swamp in the mountains on Kauai. They purposely chose a location distant from, and climatically and ecologically distinct from, the agricultural area in which the biological control agents had been introduced. The goal was to quantify the “mortality of native moths caused by alien parasitic wasps.” They collected 2112 caterpillars from two plots in the swamp. They found parasitoids in both leaf-eating caterpillars and carnivorous caterpillars. “Fifty-eight moth species (4 alien and 54 endemic) were reared from 60 plant species (47 endemic, 6 indigenous, and 7 alien). Out of 216 parasitoids reared from 2112 caterpillars collected, most (83%) were biological control agents introduced against lowland agricultural pests, followed by accidentally introduced wasps (14%). Native parasitoids were relatively rare (4%). The most common parasitoid species were the generalist braconid control agents Meteorus laphygmae, reared from at least 12 species of moths in six different families, and Cotesia marginiventris, reared from at least nine species in three families…The level of attack by alien parasitoids is estimated to be 19% in 1999 and 22% in 2000.” While some caterpillar species may be able to sustain this level of attack, it is not known how many native species had disappeared prior to the study.
Unfortunately, there has been little study of native parasitoids in Hawaii. The small number of native parasitic wasps found in this study may be due to displacement by alien parasitic wasps, or may be the result of historically low species of parasitoids on remote islands. Nonetheless, the study suggests the potential for introduced biological control agents, such as parasitic wasps, to invade nontarget ecosystems and cause significant damage to native caterpillars, and therefore, indirectly impact the ecology of native plant species.
Removal of an invasive plant can create a niche for other invasive plants
Suckling and Sforza, 2014, consider that when the removal of an invasive plant species is followed by re-invasion by a different noxious weed species, this is also an example of an indirect effect. They point out that this result is the most common type of indirect effect documented. While some treated locations may naturally return to native plant growth, the prevalence of cases in which other noxious weed species invade the treated location, points to the importance of having a plan and the resources to re-seed areas with native plant species, before treating an area with either biocontrol agents or herbicides.
Suckling and Sforza also reported on the potential for moderate to major indirect effects on non-plant species from only four biocontrol agents:
· Urophora affinis and U. quadri-fasciata (knapweed seedhead flies): target species, spotted knapweed (Centaurea maculosa); indirect effect on elevating deer mouse populations.
· Diorhabda elongata (Mediterranean tamarisk beetle): target species, salt cedar or tamarisk (Tamarix spp.); indirect effect on loss of bird nesting habitat, mainly for the endangered southwestern willow flycatcher. (However, the effects are complex and include some factors beneficial to birds, namely the beetles providing a source of food for birds).
· Rhinocyllus conicus (weevil): target species, musk thistle (Carduus nutans); indirect effect declining populations of native picture-wing flies.
· Chrysolina quadrigemina (Klamath weed beetle): target species, St. John’s wort (Hypericum perforatum); indirect effect, increasing populations of several other noxious weed species.
The northern tamarisk beetle, Diorhabda carinulata, is now restricted for use as a biocontrol agent (USFS, 2014), as the damage caused by its use can reduce nesting habitat for the southwestern willow flycatcher. The beetle has expanded its range beyond the original targeted States. Other birds also likely nest in salt cedar, and salt cedar may provide pollen for honeybees. Diverse species of Diorhabda are suited to different ranges in the Western States, but all species have generated concerns about reducing bird habitat in established stands of salt cedar.
Additional cases of indirect effects are described in the book, Biological Control, by Heimpel and Mills, 2017.
Indirect effects of invasive invertebrates
Wong, et al. (2017), looked at this issue from a different point of view. They examined the indirect impacts of insects and other invertebrates that were not purposely introduced to combat invasive plants.
They state that, "invasive insect herbivores have been responsible for the displacement of native competitors and the restructuring of native flora worldwide... More generally, invasive species impact communities by negatively affecting some species more than others (direct effects), or by altering the strength or direction of interactions among native species (indirect effects). For example, invasive herbivores can alter competitive dynamics between native plant hosts by precipitating the competitive release of less-preferred hosts..., or altering how host relative density structures herbivore impacts... However, experimental tests of these indirect effects of invasive herbivores which manifest as changes in competitive interactions between native plant hosts are lacking... The stability of competitive interactions, and ultimately, the coexistence of plant species, arise from the response of a focal plant to its neighbouring competitors... Stable coexistence is promoted when individuals of each species limit their population growth by responding more negatively to conspecific than heterospecific individuals (negative frequency dependence), whereas species that respond more positively to conspecifics (positive frequency dependence) generate unstable dynamics that can lower diversity... If competing plant species share herbivores which move between them and differentially impact their performance, the presence of herbivores could alter the relative strength of interspecific and intraspecific competition."
Wong, et al. (2017), "tested the effects of an invasive aphid herbivore, Aphis nerii, on its native congener, Aphis asclepiadis, and two closely related, co-occurring native milkweed hosts, common milkweed and butterfly milkweed. (They) tested the impact of the invasive herbivore on three aspects of the native community: (i) direct impacts on the native herbivore, (ii) direct impact on the performance of each native plant host, and (iii) indirect impacts on the competitive dynamics of the native plant hosts. (They) show that in addition to its strong direct effects, the invasive herbivore also exerts subtle, indirect impacts on plant competitive dynamics that could have long-term consequences for native community structure."
Wong, et al., state that, "Asclepias syriaca (common milkweed) and Asclepias tuberosa (butterfly milkweed) are native perennials that co-occur in old field and prairie habitats throughout eastern North America and have a suite of chemical and physical defences. Several insects specialize on Asclepias species, including two phloem-sucking aphids, A. asclepiadis and A. nerii. Aphis asclepiadis is a native specialist, while A. nerii is an invasive from the Mediterranean region that feeds on a wider diversity of plants.... (They) grew each milkweed species from seed...,, and planted seedlings in pairs in 2 litre pots in (12) treatments.... Over six weeks, (they) counted the number of aphids of each species on each plant once a week. At the end of the experiment, (they) recorded how many plants had died..., and harvested and dried dead and live biomass separately at 608C for 48 h."
"Overall, (they) found that the invasive herbivore had faster population growth and a broader diet breadth than its native competitor, and impacted the dynamics of the invaded community in three distinct ways: A. nerii (i) suppressed populations of its native competitor A. asclepiadis, (ii) reduced plant performance of both milkweed species more than its native competitor, and (iii) altered competitive dynamics between common milkweed and butterfly milkweed by amplifying the negative impacts of competing with heterospecific neighbours...."
"The invasive A. nerii had stronger negative impacts on plant performance than its native counterpart for both milkweed species. Aphis nerii reduced live biomass and survival... In contrast, A. asclepiadis did not significantly impact the performance of either milkweed species... This larger impact of A. nerii on plant performance may have arisen not only from its larger population sizes, but also as a result of high per capita feeding rates ... (They) also found that the invasive herbivore changed inter and intraspecific competitive dynamics that mediate plant coexistence... Only the invasive A. nerii affected competitive interactions between (the) two milkweed species, and, for both milkweed species, it caused the presence of a heterospecific plant neighbour to more negatively impact plant performance of the focal plant..."
"These results suggest that invasive herbivores may be more likely to induce indirect competitive effects among plants owing to the intense top-down pressure they exert... Common milkweed performed better in the presence of a heterospecific neighbour than a conspecific neighbour when grown with no aphids or only the native aphid... Therefore, in the absence of the invasive herbivore, there was a beneficial effect of competing with a heterospecific neighbour, which is often associated with the maintenance of stable local coexistence... However, when the invasive aphid was present..., this benefit of competing with a heterospecific neighbour was reduced for common milkweed... Similarly, butterfly milkweed was only negatively impacted by a heterospecific neighbour in the presence of A. nerii... These results indicate that the presence of this invasive herbivore altered the competitive dynamics between native plant species by increasing the negative impact of heterospecific neighbours... This type of dynamic, in which a species competes more strongly with heterospecific neighbours than conspecific neighbours, can lead to positive frequency dependence and unstable community dynamics."
References:
Continue with, or return to, reports on Biocontrol Agents:
Indirect impacts of biocontrol insects on native species
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, July 2020, updated December 2024.
Boettner et al., 2000, examined the indirect non-target effects of the introduction of Compsilura concinnata (a parasitoid fly introduced into North America repeatedly from 1906 to 1986, for control of gypsy moths) on native moths, including a silk moth. They deployed, in the field, larvae of two native silk moth species to examine the attack rate by Compsilura concinnata. They found high levels of parasitism in all samples studied, up to 100% in some samples. They warned that indirect non-target effects could potentially be responsible for extinctions, at least locally, of native insect species.
They also found that few studies had been done on the ecological impact of this and other introduced invertebrates, including the Asian lady beetle (Harmonta axyridis), which was introduced for biological control in the eastern US and Canada over several decades into the 1990s, and is now abundant and widespread in the US and Canada. The Asian lady beetle is now considered one of the most invasive insects. This species has resulted in the decline of native ladybird species and some other insects."
Boettner et al., 2000, warned that, as of 2000, federal requirements and funding for testing the ecological impacts of biological control agents is inadequate.
Hennemann and Memmott, 2001, warned that looking solely at direct effects on non-target plant species is not adequate to determine ecological impacts of biocontrol agents. They found that, “Indirect effects on native [insect] species are the most difficult to assess. An insect herbivore introduced to control a weed could be attacked by generalist native parasitoids that also have native hosts. If the… biological control agent is abundant, then there is the potential for apparent competition between the agent and native [insect] herbivores, mediated via shared native parasitoids. Thus, even the introduction of an entirely species-specific herbivore, presumed to have no nontarget effects, still could have a community-wide impact. Only by understanding how invasive species interact within the context of the entire community can we hope to assess the risks to native species, whether they be direct effects on single species or indirect effects on several species across trophic levels.”
“There have been at least 122 releases of parasitic wasps and flies against agricultural pest Lepidoptera in Hawaii within the past 100 years, providing high potential for nontarget effects, particularly on leaf-feeding [native] caterpillars” (Hennemann & Memmott, 2001).
Hennemann and Memmott, 2001, conducted an extensive field study of parasitoids found in moths in the remote Alakai Swamp in the mountains on Kauai. They purposely chose a location distant from, and climatically and ecologically distinct from, the agricultural area in which the biological control agents had been introduced. The goal was to quantify the “mortality of native moths caused by alien parasitic wasps.” They collected 2112 caterpillars from two plots in the swamp. They found parasitoids in both leaf-eating caterpillars and carnivorous caterpillars. “Fifty-eight moth species (4 alien and 54 endemic) were reared from 60 plant species (47 endemic, 6 indigenous, and 7 alien). Out of 216 parasitoids reared from 2112 caterpillars collected, most (83%) were biological control agents introduced against lowland agricultural pests, followed by accidentally introduced wasps (14%). Native parasitoids were relatively rare (4%). The most common parasitoid species were the generalist braconid control agents Meteorus laphygmae, reared from at least 12 species of moths in six different families, and Cotesia marginiventris, reared from at least nine species in three families…The level of attack by alien parasitoids is estimated to be 19% in 1999 and 22% in 2000.” While some caterpillar species may be able to sustain this level of attack, it is not known how many native species had disappeared prior to the study.
Unfortunately, there has been little study of native parasitoids in Hawaii. The small number of native parasitic wasps found in this study may be due to displacement by alien parasitic wasps, or may be the result of historically low species of parasitoids on remote islands. Nonetheless, the study suggests the potential for introduced biological control agents, such as parasitic wasps, to invade nontarget ecosystems and cause significant damage to native caterpillars, and therefore, indirectly impact the ecology of native plant species.
Removal of an invasive plant can create a niche for other invasive plants
Suckling and Sforza, 2014, consider that when the removal of an invasive plant species is followed by re-invasion by a different noxious weed species, this is also an example of an indirect effect. They point out that this result is the most common type of indirect effect documented. While some treated locations may naturally return to native plant growth, the prevalence of cases in which other noxious weed species invade the treated location, points to the importance of having a plan and the resources to re-seed areas with native plant species, before treating an area with either biocontrol agents or herbicides.
Suckling and Sforza also reported on the potential for moderate to major indirect effects on non-plant species from only four biocontrol agents:
· Urophora affinis and U. quadri-fasciata (knapweed seedhead flies): target species, spotted knapweed (Centaurea maculosa); indirect effect on elevating deer mouse populations.
· Diorhabda elongata (Mediterranean tamarisk beetle): target species, salt cedar or tamarisk (Tamarix spp.); indirect effect on loss of bird nesting habitat, mainly for the endangered southwestern willow flycatcher. (However, the effects are complex and include some factors beneficial to birds, namely the beetles providing a source of food for birds).
· Rhinocyllus conicus (weevil): target species, musk thistle (Carduus nutans); indirect effect declining populations of native picture-wing flies.
· Chrysolina quadrigemina (Klamath weed beetle): target species, St. John’s wort (Hypericum perforatum); indirect effect, increasing populations of several other noxious weed species.
The northern tamarisk beetle, Diorhabda carinulata, is now restricted for use as a biocontrol agent (USFS, 2014), as the damage caused by its use can reduce nesting habitat for the southwestern willow flycatcher. The beetle has expanded its range beyond the original targeted States. Other birds also likely nest in salt cedar, and salt cedar may provide pollen for honeybees. Diverse species of Diorhabda are suited to different ranges in the Western States, but all species have generated concerns about reducing bird habitat in established stands of salt cedar.
Additional cases of indirect effects are described in the book, Biological Control, by Heimpel and Mills, 2017.
Indirect effects of invasive invertebrates
Wong, et al. (2017), looked at this issue from a different point of view. They examined the indirect impacts of insects and other invertebrates that were not purposely introduced to combat invasive plants.
They state that, "invasive insect herbivores have been responsible for the displacement of native competitors and the restructuring of native flora worldwide... More generally, invasive species impact communities by negatively affecting some species more than others (direct effects), or by altering the strength or direction of interactions among native species (indirect effects). For example, invasive herbivores can alter competitive dynamics between native plant hosts by precipitating the competitive release of less-preferred hosts..., or altering how host relative density structures herbivore impacts... However, experimental tests of these indirect effects of invasive herbivores which manifest as changes in competitive interactions between native plant hosts are lacking... The stability of competitive interactions, and ultimately, the coexistence of plant species, arise from the response of a focal plant to its neighbouring competitors... Stable coexistence is promoted when individuals of each species limit their population growth by responding more negatively to conspecific than heterospecific individuals (negative frequency dependence), whereas species that respond more positively to conspecifics (positive frequency dependence) generate unstable dynamics that can lower diversity... If competing plant species share herbivores which move between them and differentially impact their performance, the presence of herbivores could alter the relative strength of interspecific and intraspecific competition."
Wong, et al. (2017), "tested the effects of an invasive aphid herbivore, Aphis nerii, on its native congener, Aphis asclepiadis, and two closely related, co-occurring native milkweed hosts, common milkweed and butterfly milkweed. (They) tested the impact of the invasive herbivore on three aspects of the native community: (i) direct impacts on the native herbivore, (ii) direct impact on the performance of each native plant host, and (iii) indirect impacts on the competitive dynamics of the native plant hosts. (They) show that in addition to its strong direct effects, the invasive herbivore also exerts subtle, indirect impacts on plant competitive dynamics that could have long-term consequences for native community structure."
Wong, et al., state that, "Asclepias syriaca (common milkweed) and Asclepias tuberosa (butterfly milkweed) are native perennials that co-occur in old field and prairie habitats throughout eastern North America and have a suite of chemical and physical defences. Several insects specialize on Asclepias species, including two phloem-sucking aphids, A. asclepiadis and A. nerii. Aphis asclepiadis is a native specialist, while A. nerii is an invasive from the Mediterranean region that feeds on a wider diversity of plants.... (They) grew each milkweed species from seed...,, and planted seedlings in pairs in 2 litre pots in (12) treatments.... Over six weeks, (they) counted the number of aphids of each species on each plant once a week. At the end of the experiment, (they) recorded how many plants had died..., and harvested and dried dead and live biomass separately at 608C for 48 h."
"Overall, (they) found that the invasive herbivore had faster population growth and a broader diet breadth than its native competitor, and impacted the dynamics of the invaded community in three distinct ways: A. nerii (i) suppressed populations of its native competitor A. asclepiadis, (ii) reduced plant performance of both milkweed species more than its native competitor, and (iii) altered competitive dynamics between common milkweed and butterfly milkweed by amplifying the negative impacts of competing with heterospecific neighbours...."
"The invasive A. nerii had stronger negative impacts on plant performance than its native counterpart for both milkweed species. Aphis nerii reduced live biomass and survival... In contrast, A. asclepiadis did not significantly impact the performance of either milkweed species... This larger impact of A. nerii on plant performance may have arisen not only from its larger population sizes, but also as a result of high per capita feeding rates ... (They) also found that the invasive herbivore changed inter and intraspecific competitive dynamics that mediate plant coexistence... Only the invasive A. nerii affected competitive interactions between (the) two milkweed species, and, for both milkweed species, it caused the presence of a heterospecific plant neighbour to more negatively impact plant performance of the focal plant..."
"These results suggest that invasive herbivores may be more likely to induce indirect competitive effects among plants owing to the intense top-down pressure they exert... Common milkweed performed better in the presence of a heterospecific neighbour than a conspecific neighbour when grown with no aphids or only the native aphid... Therefore, in the absence of the invasive herbivore, there was a beneficial effect of competing with a heterospecific neighbour, which is often associated with the maintenance of stable local coexistence... However, when the invasive aphid was present..., this benefit of competing with a heterospecific neighbour was reduced for common milkweed... Similarly, butterfly milkweed was only negatively impacted by a heterospecific neighbour in the presence of A. nerii... These results indicate that the presence of this invasive herbivore altered the competitive dynamics between native plant species by increasing the negative impact of heterospecific neighbours... This type of dynamic, in which a species competes more strongly with heterospecific neighbours than conspecific neighbours, can lead to positive frequency dependence and unstable community dynamics."
References:
- Boettner, G.H., Elkinton, J.S., & Boettner, C.J. (Dec., 2000). Effects of a biological control introduction on three nontarget native species of Saturniid moths. Conservation Biology, 14(6): 1798-1806.
- Heimpel, G.E, & Mills, N.J. (2017). Biological Control: Ecology and Applications. Cambridge: Cambridge University Press.
- Henneman, M.L., & Memmott, J. (Aug. 17, 2001). Infiltration of a Hawaiian community by introduced biological control agents. Science, New Series, 293 (5533), 1314-1316.
- Suckling, D.M., & Sforza, R.F.H. (January, 2014). What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9(1).
- Wong, L., Grainger, T.N., Start, D., & Gilbert, B. (2017). An invasive herbivore structures plant competitive dynamics. Biology Letters, 13, 1-4.
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