Research Article |
Corresponding author: Johannes Le Roux ( jaco.leroux@mq.edu.au ) Academic editor: Alain Roques
© 2019 Jarryd D. Foster, Allan G. Ellis, Llewellyn C. Foxcroft, Scott P. Carroll, Johannes Le Roux.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Foster JD, Ellis AG, Foxcroft LC, Carroll SP, Le Roux JJ (2019) The potential evolutionary impact of invasive balloon vines on native soapberry bugs in South Africa. NeoBiota 49: 19-35. https://doi.org/10.3897/neobiota.49.34245
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Following their establishment in new communities, invasive species may cause evolutionary changes in resident native species. This is clearly true for phytophagous insects, which may adapt rapidly when utilising abundant and widespread introduced hosts. The balloon vines Cardiospermum halicacabum and C. grandiflorum were introduced to South Africa approximately 100 years ago and are classified as minor and major weeds, respectively. Here we assess the potential evolutionary impact of these vines on native Leptocoris soapberry bug populations in Kruger National Park (KNP), using phylogenetic and morphometric analyses. We found that soapberry bugs associated with C. halicacabum are genetically and morphologically distinct from those associated with C. grandiflorum. This suggests that native soapberry bugs in KNP exhibit some degree of host preference, indicating that these vines may have had significant evolutionary consequences for these insects. The proboscis length of soapberry bugs feeding on C. halicacabum closely matched fruit size, often being longer than fruit size at the population level. These soapberry bugs are therefore well-suited to feeding on this introduced plant species.
Balloon vine, Cardiospermum, invasive species, Kruger National Park, Leptocoris, rapid evolution, soapberry bug
Evolved and plastic changes are important not only for the colonization and spread of non-native species but are also prevalent in native species as they respond to the presence of introduced taxa (
The genus Cardiospermum L. (Sapindaceae), commonly known as balloon vines, consists of 17 mainly Neotropical species (
Two soapberry bug genera are native to southern Africa, namely Leptocoris and Boisea, the former being more widely distributed (
In this study, we used phylogenetic analyses, in combination with morphometric measurements, to investigate the potential evolutionary impact of invasive C. halicacabum and C. grandiflorum on native soapberry bugs (genus Leptocoris) in South Africa. To examine whether any evolved differentiation might have resulted from contemporary natural selection, the proboscis lengths of Leptocoris mutilatus Gers. were measured with respect to fruit size variation in invasive C. halicacabum populations. The expectation was that soapberry bug proboscis lengths will closely match fruit size in C. halicacabum and that any shifts in proboscis lengths will correspond to variation in seed capsule (balloon) size in C. halicacabum populations.
Thirteen populations of C. halicacabum and a single C. grandiflorum population were identified in Kruger National Park (KNP; Suppl. material
To confirm the putative Leptocoris mutilatus species assignment of soapberry bugs feeding on invasive Cardiospermum in KNP, individuals collected from C. halicacabum and C. grandiflorum populations were selected for phylogenetic analyses (Suppl. material
The mitochondrial cytochrome c oxidase subunit I (COI) gene was amplified using the universal primers LCOI-1490 (5’-GGT CAA CAA ATC ATA AAG ATA TTG G-3’) and HCOI-2198 (5’-TAA ACT TCA GGG TGA CCA AAA AAT CA-3’) (
All PCR products were purified using the QIAquick PCR Purification Kit (Qiagen, supplied by Whitehead Scientific, Cape Town, South Africa). Purified products were sequenced using an ABI 3730 XL automated machine (Central Analytical Facilities, Stellenbosch University, South Africa).
DNA sequence data were aligned using CLUSTALW version 2.1 (
A phylogeny was reconstructed using Bayesian inference (BI) and maximum likelihood (ML) approaches. Bayesian inference was conducted using MRBAYES version 3.2.6 (
Maximum likelihood analysis was conducted using GARLI version 2.01 (
To investigate whether soapberry bug proboscis lengths track fruit size variation in C. halicacabum populations, a total of 311 full-sized fruit and 154 associated soapberry bug individuals were measured from 13 C. halicacabum populations in KNP. 20–25 fruit and 5–16 soapberry bugs were measured for each population (Suppl. material
Interior of fruiting capsule of balloon vine C. halicacabum. The upper portion of the capsule wall has been trimmed away and shows the central position of the seeds. The ‘fruit size’ variable we measured was the shortest distance from the fruit capsule perimeter to the seed coat for each seed. The second species in this study, Cardiospermum grandiflorum, has larger fruits of similar architecture (Image source: Wikimedia commons: Cardiospermum halicacabum).
ANCOVA models were used to quantify and compare proboscis-body size allometries between bugs found on different Cardiospermum hosts. For those bugs found on C. halicacabum, regression analysis was used to determine whether there was a significant trait-matching relationship between mean population proboscis lengths and mean population fruit sizes. A two-sample t-test was used to determine whether mean proboscis length was significantly different between bugs found on C. grandiflorum and C. halicacabum. A Kruskal-Wallis rank sum test and post-hoc Dunn’s test were used to compared proboscis lengths at the population level. Two-sample t-tests were also used to determine whether fruit size was significantly different between balloon vine species. Furthermore, two-sample t-tests were used to determine the nature and direction of the morphological fit between the fruit sizes of each Cardiospermum host and the proboscis lengths of their associated soapberry bug predators.
All statistical analyses were conducted in R (
The aligned COI dataset contained 545 base pairs. All sequences were deposited into the GenBank online repository.
The phylogeny recovered well-supported basal clades for Leptocoris vicinus and L. aethiops, and a larger clade containing L. amictus and L. hexophtalmus (Figure
Bayesian phylogeny based on COI DNA sequencing data illustrating phylogenetic relationships among African Leptocoris species. Shaded branches refer to Leptocoris specimens collected from Cardiospermum halicacabum and C. grandiflorum in Kruger National Park. Nodal support is shown as posterior probabilities and bootstrap values above and below the branches, respectively.
There was a significant positive relationship between proboscis length and thorax width for both halicacabum (p < 0.001; Table
Linear regressions showing the relationship between proboscis length and thorax width for adult Leptocoris mutilatus found in association with Cardiospermum halicacabum and C. grandiflorum. Each point represents an individual.
Linear regressions showing the relationship between proboscis length and body length for adult Leptocoris mutilatus found in association with Cardiospermum halicacabum and C. grandiflorum. Each point represents an individual.
Details of the models used to quantify and compare allometries of soapberry bugs in KNP, and to assess the relationship between population means of halicacabum bug proboscis length (in mm) and C. halicacabum fruit size (in mm).
LM (Proboscis length ~ Thorax width * Host plant) | ||||
Estimate | SE | t-value | p-value | |
(Intercept) | 1.6628 | 0.4718 | 3.524 | < 0.001 |
Thorax width | 1.5029 | 0.1436 | 10.467 | < 0.001 |
Host C. grandiflorum | 2.8979 | 0.8949 | 3.238 | < 0.01 |
Thorax width: Host C. grandiflorum | -1.0584 | 0.2565 | -4.126 | < 0.001 |
Residual SE: 0.439 on 180 df | ||||
Multiple r2: 0.4371, Adjusted r2: 0.4277 | ||||
F-statistic: 46.59 on 3 and 180 df, p-value: < 0.001 | ||||
LM (Proboscis length ~ Body length * Host plant) | ||||
Estimate | SE | t-value | p-value | |
(Intercept) | 2.1152 | 0.5319 | 3.977 | < 0.001 |
Body length | 0.3799 | 0.0451 | 8.431 | < 0.001 |
Host C. grandiflorum | 3.0109 | 0.9499 | 3.170 | < 0.01 |
Body length: Host C. grandiflorum | -0.2989 | 0.0770 | -3.883 | < 0.001 |
Residual SE: 0.4734 on 180 DF | ||||
Multiple r2: 0.3454, Adjusted r2: 0.3345 | ||||
F-statistic: 31.66 on 3 and 180 df, p-value: < 0.001 | ||||
LM (Mean proboscis length ~ Mean fruit size) | ||||
Estimate | SE | t-value | p-value | |
(Intercept) | 6.8366 | 0.7885 | 8.671 | < 0.001 |
Mean fruit size | -0.0411 | 0.1262 | -0.326 | > 0.05 |
Residual SE: 0.1832 on 11 DF | ||||
Multiple r2: 0.0095, Adjusted r2: -0.0805 | ||||
F-statistic: 0.1062 on 1 and 11 df, p-value: > 0.05 |
There was no significant relationship between population means of C. halicacabum fruit size and proboscis lengths of their associated soapberry bug predators (p > 0.05; Table
Relationship between proboscis length and fruit size (distance from balloon exterior to nearest seed coat) for soapberry bugs and their associated balloon vine host species in Kruger National Park. Each point represents a single population and error bars are ±SD.
Difference between average proboscis length and average fruit size (i.e. proboscis length - fruit size) for Leptocoris mutilatus and Cardiospermum populations in KNP. Green bars represent populations in which soapberry bugs are well-suited to feed on their Cardiospermum hosts (i.e. proboscis length > fruit size) and red bars represent populations in which soapberry bugs are poorly matched (i.e. proboscis length < fruit size).
Grand means (±SD) of proboscis length and body size measures (in mm) of soapberry bugs in KNP, and fruit sizes (in mm) of their Cardiospermum hosts.
Host plant | Proboscis length (mm) | Thorax width (mm) | Body length (mm) | Fruit size (mm) |
---|---|---|---|---|
Cardiospermum halicacabum | 6.59 ± 0.59 | 3.28 ± 0.25 | 11.77 ± 0.85 | 6.24 ± 0.80 |
Cardiospermum grandiflorum | 6.14 ± 0.34 | 3.56 ± 0.38 | 12.54 ± 1.41 | 7.62 ± 0.72 |
This study aimed to assess the potential for impacts by invasive balloon vines on morphological traits of native soapberry bug (genus Leptocoris) populations in South Africa’s flagship protected area, Kruger National Park (KNP). We found L. mutilatus bugs on both invasive host plants and provide some evidence for genetic and morphological differentiation between bugs feeding on different balloon vine species in KNP. Additionally, the proboscis-fruit size trait-matching patterns differed between the two balloon vines. Halicacabum bugs had proboscis lengths well-suited for feeding on the seeds of intact fruits, but this was not the case for grandiflorum bugs.
Genetic differentiation between soapberry bug populations associated with C. halicacabum and C. grandiflorum in KNP (Figure
The lack of a significant proboscis length-fruit size trait-matching relationship across halicacabum bug populations (Figure
While the fit between proboscis length and fruit size is likely adaptive (
Interestingly, the average proboscis length of grandiflorum bugs was 1.48 mm shorter than the average fruit size of the associated C. grandiflorum population, indicating that these bugs are less well-suited to feed on these fruits. This may imply that these bugs have recently colonised this balloon vine such that selection has not had long to act (
Not knowing about the potentially illuminating influences of native Sapindaceae fruit size on the allometries of halicacabum and grandiflorum bugs is a key shortcoming in this study, and any ongoing local patterns of host-associated differentiation inferred here may be changed by plant eradication efforts. Despite these challenges, our findings add support to considerations of the potentially significant evolutionary impact of introduced balloon vines on native soapberry bug populations, and that these impacts may be dissimilar for different balloon vine species. More extensive sampling in South Africa of soapberry bugs from both introduced balloon vine species and native sapindaceous species is needed to determine the degree of morphological and genetic differentiation between invasive- and native-feeding soapberry bug populations. This will provide a more complete assessment of the potential evolutionary impact of introduced balloon vines on soapberry bug populations, and the potential for these bugs as neoclassical biocontrol of Cardiospermum invasions.
Financial support was provided by the DST-NRF Centre of Excellence for Invasion Biology. The authors are grateful for sampling permits from South African National Parks. JF thanks Thembeka Thwala, Annoit Mashele, Martin Sarela and Isaac Sedibe for their protection, assistance and laughs in the field; Megan Mathese for lab assistance. LF acknowledges South Africa’s National Research Foundation (Project Numbers IFR2010041400019 and IFR160215158271).
Tables S1–S5.
Data type: measurements
Explanation note: Table S1. Sampling localities for Cardiospermum populations included in this study. Table S2. Locality data for Leptocoris species included in this study. Table S3. Number of fruit and soapberry bugs measured per population. Table S4. Population-level comparisons of proboscis length-body size allometries between halicacabum and grandiflorum bugs using ANCOVA models.Table S5. Details of the linear models used to assess the relationship between population means of the halicacabum bug allometry residuals (in mm) and C. halicacabum fruit size (in mm).