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. 2019 Sep 4;15(9):20190470. doi: 10.1098/rsbl.2019.0470

Human-mediated disturbance in multitrophic interactions results in outbreak levels of North America's most venomous caterpillar

Glen R Hood 1,3,✉, Mattheau Comerford 3, Amanda K Weaver 3, Patricia M Morton 2, Scott P Egan 3,✉
PMCID: PMC6769147  PMID: 31480937

Abstract

Anthropogenic environmental change is predicted to disrupt multitrophic interactions, which may have drastic consequences for population-level processes. Here, we investigate how a large-scale human-mediated disturbance affects the abundance of North America's most venomous caterpillar species, Megalopyge opercularis. Specifically, we used a natural experiment where netting was deployed to cover the entire canopies of a subset of mature southern live oak trees (Quercus virginiana) to exclude urban pest birds (grackles and pigeons), throughout an 8.1 km2 area encompassing a medical centre in Houston, Texas. We used this experimental exclusion to test the following hypothesis: release from avian predators increases caterpillar abundance to outbreak levels, which increases the risk to human health. Results from a multi-year survey show that caterpillar abundance increased, on average, more than 7300% on netted versus non-netted trees. Thus, increases in caterpillar abundance due to anthropogenic enemy release increase human exposure to this venomous pest, and should be considered a health threat in the area. This study emphasizes the unforeseen consequences of ecological disturbance for species interactions and highlights the importance of considering ecology in urban planning.

Keywords: asp, anthropogenic disturbance, Megalopyge opercularis, top-down control

1. Introduction

In the last approximately 250 years, about 83% of the Earth's land surface has been altered to grow crops, raise animals, obtain timber and build cities [1]. As a consequence, the effects of landscape modification and habitat disturbance have recently become major research themes in ecology, evolution and conservation biology [2–8]. The collective findings demonstrate that habitat modification can disrupt the delicate balance between ecological interactions required for species existence, resulting in patterns of species loss that are global in scale and taxonomically wide-spread [2–5]. However, one alternative to species loss posits that the abundance of individuals within population can reach ‘outbreak' levels in disturbed habitats [9]. Species at lower or intermediate trophic levels, such as plant-feeding insects, are especially prone to outbreaks triggered by release from natural enemies [6,10,11]. This release is often associated with a reduction in suitable habitat for natural enemies, such as predators or parasites, in modified compared with non-modified environments [6,10–13].

The effects of enemy release on herbivore abundance may be further magnified when modification to habitats directly affects the way in which organisms interact [14–16]. In this scenario, not only can suitable habitat for enemies be further reduced, but in extreme cases, natural enemies can be completely excluded from attacking herbivores in previously shared environments. For example, it is common for urban-planning strategies to completely exclude birds from using ornamental plants and building structures, and this practice is global in scale [17,18]. The exclusion of avian predators in these environments may increase abundance of herbivores naturally controlled in non-modified urban areas.

Here, we investigate such a scenario involving North American's most venomous caterpillars, Megalopyge opercularis, which possesses severe detriments to human health (see §2a ‘Study system’ for pathology). In Houston, TX, USA, netting deployed around the canopy of oak trees to exclude urban pest birds may have unintended consequences for caterpillars feeding on these trees. We take advantage of this exclusion experiment to test how anthropogenic environmental change (habitat modification and ecological disturbance) can affect interactions between species across trophic levels. Specifically, we test the hypothesis that release from avian predation increases abundance of this venomous pest that can negatively affect human health. Our study represents a case where enemy release drastically increases caterpillar abundance, thereby increasing the risk of human exposure to this venomous species, emphasizing the unforeseen consequences of disrupting the ecology of interacting species.

2. Material and methods

(a). Study system

The southern flannel moth, Megalopyge opercularis (Lepidoptera: Megalopygidae), also referred to in its juvenile stage as the ‘puss caterpillar' or ‘asp' (figure 1a), is endemic to the southern USA [19], where it has two generations per year and feeds on at least 41 plant genera [20]. The caterpillar, one of the continent's most venomous [21,22], is covered in a coat of tawny-coloured hairs hiding clusters of needle-like spines (modified setae) connected to venom glands defending against predators (figure 1b) [23–25]. Despite the presence of spines, caterpillars are attacked by parasitoids and pupae are predated by lacewings, spiders and anoles [24,25]. Lepidopterists historically have not considered avian predation a source of asp mortality owing to their physical and chemical defence. However, three members of our authorship team have directly observed blue jays (Cyanocitta cristata), great-tailed grackles (Quiscalus mexicanus) and downy woodpeckers (Picoides pubescens) feeding on asp pupae on 10 different occasions at our study site, suggesting that avian predation may be an important and overlooked source of mortality and top-down control.

Figure 1.

Figure 1.

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(a) Asp on a live oak leaf. (b) Venomous spines hidden underneath hairs and (c) a rash caused by asp envenomation. (d,e) Netted trees in the Texas Medical Centre (TMC) protected from bird predation. (f) Map of the study area including non-netted trees at Rice University (RU), Southgate neighbourhood (SG) and Hermann Park (HP) (yellow) and both netted and non-netted trees TMC (red). Note that because the mesh size (2.54 cm2) is approximately as large as the asps (2.4–3.6 cm), the detection probability did not differ between netted and non-netted trees.

Owing to the caterpillars' broad geographical distribution and diet, it is often encountered by humans in urban environments and considered a seasonal health hazard by medical professionals [22]. When humans contact caterpillar spines, the sting can induce a ‘burning pain' at the site of envenomation described as being similar to a broken bone or blunt force trauma [26] (figure 1c). Additionally, systemic signs of a sting include headaches, nausea, vomiting, fever, low blood pressure, inflammation of lymph nodes, and in severe cases, abdominal distress, muscle spasms, convulsions and respiratory stress [27–31]. Despite the severity of health issues associated with stings, ‘…health care professionals have never seen nor heard of the creature…[and] victims are left with the distress of an unknown prognosis' [22, p. 4].

The species can also reach outbreak levels. For example, public schools in Texas were temporarily closed owing to outbreaks in San Antonio and Galveston in 1923 and 1951, respectively [30]. Recent reports of asp stings have increased in the southern USA, and specifically in Texas, where the number of cases from 2003 to 2006 was an order of magnitude greater than in any other state [22]. Records from Rice University Health Center at our study location in Houston, Texas, revealed an increase in stings in autumn 2016, resulting in approximately 50–60 cases, an average of three per day.

(b). Experimental design

There are hundreds of large, mature southern live oaks planted as landscape ornamentals across the Texas Medical Center (TMC) in downtown Houston, Texas (29°41′39.5928″ N, 95°24′03.9312″ W). At least 6 years ago, canopies of a subset of trees in the TMC were individually covered in netting to deter use of urban pest bird such as grackles and pigeons that deface the buildings, sidewalks and greenspaces in the TMC (figure 1d,e). These protected (netted) and unprotected (non-netted) trees coexist along streets, sidewalks and in greenspaces. The TMC is at the centre of an 8.1 km2 area surrounded by Rice University (RU), which is a designated arboretum, to the northeast (29°43′01.0056″ N, 95°24′21.0852″ W), Southgate neighbourhood (SG) to the southwest (29°42′42.8364″ N, 95°24′25.9668″ W), and Hermann Park (HP) to the east (29°42′43.8192″ N, 95°23′15.5184″ W), populated with hundreds of non-netted live oaks (figure 1f). We used this matrix of netted and non-netted trees to determine the effect of excluding birds on the abundance of asp larvae and pupae.

In 2015, 2017 and 2018, during an 18-day period from 16 October to 3 November, between the hours of 9.00 and 16.00, during peak seasonal and daily larval feeding activity [22], we surveyed a total of 438 trees, both netted and non-netted at TMC (2015: 18 netted, 19 non-netted; 2017: 69 netted, 23 non-netted; 2018: 62 netted, 40 non-netted) and non-netted trees at RU (2017: 70; 2018: 73), SG (2018: 32) and HP (2018: 32) for asps. In 2018, 12 of the trees at TMC had been netted the previous years (removed spring 2018). In early October of each year of the study, a subset of caterpillars were identified using the characteristics in [24] to confirm species status. At each tree, for approximately 10 min, we searched for and counted the number of caterpillars and newly formed pupae on trunks, branches and leaves.

To account for potential temporal and spatial heterogeneity, we compared the abundance of asp on netted versus non-netted trees using negative binomial regression models, ideal for count data with overdispersion (indicated by a significant likelihood ratios test). We performed four analyses to compare asp abundance between (a) netted and non-netted trees across three years (2015, 2017, 2018) at TMC only (model 1), (b) non-netted trees at RU and netted and non-netted trees at TMC in 2017 and 2018 (model 2), (c) non-netted trees at RU, SG and HP and netted and non-netted trees at TMC in 2018 only (model 3), and (d) netted, non-netted, and previously netted trees at TMC in 2018 only (model 4). All pairwise comparisons of means within each model were conducted using Tukey's post hoc analyses (adjusted for multiple comparisons) of estimated marginal means.

3. Results

The number of caterpillars observed on live oaks was greater on netted (mean across years = 38.1074 ± 3.1737; range: 0–285) versus non-netted trees (0.5090 ± 0.031; range: 0–18). At TMC only (model 1), the abundance of caterpillars differed between netted and non-netted trees within and between years and in two cases, between years on netted trees (figure 2a and table 1). Similarly, caterpillar abundance at RU and TMC (model 2) differed between netted and non-netted trees within and between years and sites (figure 2b and table 1). At all four sites in 2018 (model 3), the abundance of caterpillars was not significantly different between individual non-netted trees, but differed between netted and non-netted trees within and between sites (figure 2c, table 1). These significant differences were driven by an approximately 73% increase in the number of non-netted trees where no caterpillars were observed. Of the 277 non-netted trees surveyed, 218 (78.70%) contained no caterpillars, while only 9 of 149 netted trees (6.04%) at TMC contained no caterpillars. Lastly, the abundance of caterpillars differed significantly between non-netted and previously netted trees and non-netted and netted trees, but not between previously netted and netted trees (model 4; figure 2d and table 1), suggesting that a lag exists between when nets are removed and when birds have observable impacts on caterpillar abundance.

Figure 2.

Figure 2.

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Boxplots comparing caterpillar abundance (mean ± s.e.) on netted and non-netted trees (a) across years at TMC only (model 1), (b) between two sites (RU, TMC) across 2 years (2017, 2018) (model 2), (c) between netted trees at TMC and three surrounding non-netted sites (SG, RU, HP) in 2018 (model 3), and (d) netted, non-netted and previously netted trees at TMC in 2018 only (model 4). Within panels, boxplots not sharing the same letter(s) are significantly different (p < 0.05; table 1).

Table 1.

Results from four negative binomial regressions comparing abundance of caterpillars on netted, non-netted and previously netted trees (significant values are in italics). Values in the ‘estimate' column are exponentiated.

model predictor estimate z-value p-value
1 intercept 46.090 23.237 <0.0001
2017 0.770 −1.411 0.158
2018 0.365 −3.808 0.0001
non-netted 0.042 −15.626 <0.0001
2 intercept 56.969 27.737 <0.0001
RU non-netted 2017 0.001 −13.644 <0.0001
RU non-netted 2018 0.004 −17.301 <0.0001
TMC non-netted 2017 0.058 −9.444 <0.0001
TMC non-netted 2018 0.010 −12.757 <0.0001
TMC netted 2017 0.449 −3.975 <0.0001
3 intercept 56.969 31.020 <0.0001
HP non-netted 0.007 −13.651 <0.0001
RU non-netted 0.004 −13.980 <0.0001
SG non-netted 0.006 −13.654 <0.0001
TMC non-netted 0.010 −13.492 <0.0001
4 intercept 56.698 33.201 <0.0001
non-netted 0.010 −13.906 <0.0001
previously netted 0.911 −0.307 0.759
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4. Discussion

Overall, we demonstrated a greater than 7300% increase in the abundance of North America's most venomous caterpillar when birds were excluded, a pattern consistent across space and time. Ominously, these caterpillars are on trees that line the greenspaces, sidewalks, and streets of the TMC, the largest medical centre in the world, in the fourth largest city in the USA. The TMC employs over 106 000 health care professionals that service more than 160 000 patients daily [32]. Given the sensitive nature of the patient population, increases in caterpillar abundance likely translate to increases in human exposure and should be considered a threat in the area.

Increased asp abundance is problematic for an additional reason: humans may not be the only species at risk. The Houston Zoo, located on the northeast perimeter of the TMC, houses over 6000 animals from 900 different species. Many zoos use netting to cover animal enclosures and observation areas, which could facilitate similar outbreaks and increase animal and human exposure. In fact, increased caterpillar abundance at an Austin, Texas zoo has recently caused concern for the animal population and patrons [33]. To our knowledge, no recorded accounts of non-human animal stings exist; however, dogs experimentally injected with venom extracts displayed increased blood pressure and respiration [34].

We postulate that the increase in caterpillar abundance on netted trees is a direct effect of removing an apex predator (birds) and not the result of the indirect effect of reducing bird predation on other natural enemies of the caterpillar. If the latter were true, such cascades would ultimately result in the decrease in caterpillar abundance, the opposite effect of our observed outcome. Additionally, preliminary data show that parasitoid levels between netted and non-netted trees did not differ, which suggests birds as the primary source of top-down control in this situation. However, we cannot rule out the possibility that the netting treatment has shifted bird predation behaviour in a way that has increased predation on natural enemies that move between trees, such as anoles. If birds are forced to feed on ground-dwelling lizards that hunt in the trees instead of caterpillars, we would predict reductions in the amount of predation by lizards leading to sudden elevations in caterpillar abundance on non-netted trees.

We have also observed additional effects of bird exclusion in our study area, and hypothesize about other consequences given the contrast in asp abundance on netted versus non-netted trees. First, we recently investigated the effects of avian predation on a gall-forming wasp and found that bird attack of galls was reduced by approximately 96% on a subset of the same netted versus non-netted trees. Second, the presence of nets on live oaks may have gradually reduced avian presence locally. Several studies show that birds can learn to avoid poor quality habitats [35], and we often observe birds at TMC in non-netted trees (next to netted trees), albeit at reduced abundance compared with surrounding non-netted areas. Third, while we recognize that high abundances in one year may not always translate to higher survival in the subsequent years, our results suggest that asp abundance on netted trees is increasing across years (figure 2a). However, outbreaks of populations of herbivorous insects are typically separated by periods of low abundance due to crashes resulting from over-exploitation of limited resources [36]. Given the artificial exclusion of avian predators, how might asp populations return to low levels of abundance on netted trees? Asp caterpillars are parasitized by flies and wasps, which can be a significant source of mortality, reaching levels of 50% [24,25]. Thus, increased effects on asp mortality from parasitism to counter the effects from avian predation may result in fluctuations in abundance typical of herbivores prone to outbreak [36]. Indeed, preliminary results suggest that parasitism of asp pupae from tachinid flies are high on netted trees (44%).

Urban areas often represent ‘ecological traps' where species are forced to settle for reduced quality habitat or resources [37]. Netted trees may represent such a case where increased caterpillar abundance results in increased intraspecific competition for limited or reduced quality resources (food, oviposition sites). Additionally, the adult wingspan ranges from 2.4 to 3.6 cm [19], mostly exceeding the net size (2.54 cm2). Preliminary observations suggest that after metamorphosis, moths may be stuck inside netted areas and forced to mate and oviposit in a bird-free space. If true, asps on individual trees may represent inbred ‘subpopulations' or ‘demes' compared with more outcrossing populations using non-netted trees. If this scenario were true, we hypothesize that a small number of moths were enclosed on the trees when nets were initially deployed, seeding the present-day populations counted therein. As a result, asps on netted trees may be stuck in an ‘evolutionary trap' as well, where they are maladapted to further environmental change owing to the effects of reduced genetic variation [37].

In conclusion, we present evidence linking increased abundance of a highly venomous caterpillar to release from avian predation. This decrease in avian predation is a direct consequence of urban planning targeted at reducing human exposure to pest birds in a metropolitan area. As a result, increases in caterpillar abundance likely increase human exposure to one of the most venomous caterpillars in North America. While we acknowledge that urban environments present a challenge to species, integrating ecology and natural history into urban planning is critical. Our study highlights the role that anthropogenic change may have for ecological interactions in modified environments and emphasizes how urban-planning choices, even when made with the best intentions, can prove dangerous without careful consideration.

Supplementary Material

Raw Data
rsbl20190470supp1.xlsx (31.8KB, xlsx)

Data accessibility

The raw data is available on Dryad (https://doi.org/10.5061/dryad.gf7hc1r) [38].

Authors' contributions

S.P.E., A.K.W., M.C. and G.R.H. conceived the study and collected data, G.R.H. and P.M.M. conducted analyses, G.R.H. wrote the manuscript and all authors edited and revised drafts. All authors approved the final version of the manuscript and agree to be held accountable for the content therein.

Competing interests

We declare we have no competing interests.

Funding

We received no funding for this study.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. Hood GR, Comerford M, Weaver AK, Morton PM, Egan SP. 2019. Data from: Human-mediated disturbance in multitrophic interactions results in outbreak levels of North America's most venomous caterpillar Dryad Digital Repository. ( 10.5061/dryad.gf7hc1r) [DOI] [PMC free article] [PubMed]

Supplementary Materials

Raw Data
rsbl20190470supp1.xlsx (31.8KB, xlsx)

Data Availability Statement

The raw data is available on Dryad (https://doi.org/10.5061/dryad.gf7hc1r) [38].

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