Research Article |
Corresponding author: Mohammadreza Lashkari ( mr.lashkari@gmail.com ) Academic editor: Pavel Stoev
© 2018 Roghayeh Shamsi Gushki, Mohammadreza Lashkari, Saeid Mirzaei.
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:
Gushki RS, Lashkari M, Mirzaei S (2018) Identification, sexual dimorphism, and allometric effects of three psyllid species of the genus Psyllopsis by geometric morphometric analysis (Hemiptera, Liviidae). ZooKeys 737: 57-73. https://doi.org/10.3897/zookeys.737.11560
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Jumping plant lice (Hemiptera: Psylloidea) are considered important vectors of plant diseases and also economically important pests in agriculture and forest ecosystems. Three psyllid species Psyllopsis repens Loginova, 1963, Psyllopsis securicola Loginova, 1963, and Psyllopsis machinosus Loginova, 1963 associated with the ash tree Fraxinus are morphologically very similar. So far, their distinction has been possible only by comparing their male and female genitalia. In this research, forewing shape and size characteristics, sexual dimorphism and their allometric effects, using geometric morphometric analysis, were examined for identification purposes. The results showed significant differences in wing shape and size between the species studied. Based on the results, two species P. machinosus and P. securicola can be differentiated with the vein M1+2, as in P. securicola the vein M1+2 is located between Rs and M3+4 veins, but the vein M1+2 is closer to the vein M3+4 in P. machinosus; also, P. repens can be differentiated from the two species P. machinosus and P. securicola by vein M. Hence, the veins M1+2, M3+4, Rs and M were the most important wing characters for discrimination of the three species, especially in the field. The analysis also showed significant differences in wing shape and size between male and female of the three species, and the allometric analysis showed that significant shape differences still remain in constant size in P. machinosus and P. repens. Geometric changes in the forewings of both sexes for the three species are illustrated.
Diaphorinini , diversity, Euphyllurinae , jumping plant lice, Liviidae
Psyllids (Hemiptera: Psylloidea) are considered as important vectors of plant diseases and economically important pests in agricultural and forest ecosystems (
Psyllopsis Low, 1879 is a small Palaearctic genus comprised of 11 species in the world, which are introduced with various species of ash (Fraxinus spp., Oleaceae). Psyllopsis genus is currently classified in the family Liviidae, sub-family Euphyllurinae, and tribe Diaphorinini (
Among the genus Psyllopsis, several species are distributed in Central Asia, such as Psyllopsis repens Loginova, 1963, which has been known from Afghanistan, Armenia, Azerbaijan, Caucasus, Iran, Serbia, Turkey (
Psyllopsis species have a similar adult morphology (
Morphological differences between males versus females sometimes cause highly intraspecific variation in Psylloidea. These variations have been specially shown in body size and color and also wing size and color (
Geometric morphometric analysis (GMA) comprises a powerful tool to study size and shape. As a technology, it has been known to detect similarities and differences between morphological structures. Numerous studies have been conducted to describe the geometric differences between different populations in Iran (
In this research, wing shape and size, sexual dimorphism and their allometric effects of the three species of the genus Psyllopsis are studied for identification purposes, which are useful in pest management programs. Therefore, the following questions have been set out, to answer whether: 1) wing geometry can help us to identify the three ash psyllids P. repens, P. securicola, and P. machinosus; and, on the other hand, is there a specific wing geometric characteristic for each species? 2) Is there sexual dimorphism in the wing shape and size of the three ash psyllids?
The adults of three species of ash psyllids, P. repens, P. securicola, and P. machinosus were collected from infected ash trees in Kerman province, Iran, in 2015. The place of collection was located in the western part of Kerman province (Bahramjerd) at 29°55'55"N, 56°40'27"E and at 2076 m a.s.l., for P. repens and P. securicola; and at 29°52'16"N, 56°57'17"E and at 2102 m a.s.l., for P. machinosus. The number of specimens for each species was chosen at more than 2P-4, which is equal to the number of variables in partial warp matrix including the uniform component (W matrix), where P is the number of landmarks (Zelditch et al. 2004). Therefore, 60 specimens including adult male and female from each species were randomly selected as sample size, which is more than the number of variables in W matrix. The right forewing of each specimen was used to prepare microscopic slides (using Canada balsam) and the photos were captured by a stereomicroscope, coupled with a digital camera. All the photos were captured with 40× magnification.
In geometric morphometric analysis, a total of eleven homologous landmarks, Type 1, were selected on the forewing (Fig.
One-way MANOVAs were designed to detect any significant differences in wing shape between species. An ANOVA procedure and Tukey pair-wise comparisons were used to detect differences in centroid size between the three species. A regression, shape on size variables, and a MANCOVA were designed to detect any allometric growth and separate allometric trajectories. Statistical analyses were performed in NTSYS-pc (
The specimens were deposited in the Psylloidea Collection of the Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran.
In this study, according to the results of MANOVA, significant differences were found in the wing shape of male/female wings in all psyllid species (Tab.
Wings in females of P. machinosus and P. repens are wider and longer than those in males; the main changes in P. machinosus and P. repens are related to the veins Rs (Landmark 1) and slightly M1+2 (Landmark 2), which are longer in females and tend to be more longer on apical edges (Figs
The size comparisons showed significant differences between wing size of the female and the male in all the species studied (F = 115.31, P < 0.0001) (Fig.
Allometric analysis showed allometric growth among female and male individuals (Tab.
The superimposition of the forewing landmarks of the three species of ash psyllid species P. repens, P. securicola, and P. machinosus adults showed a range of variation at each landmark, especially Landmarks 1, 2, and 6 (Fig.
The first two relative warps explained 45.70% and 16.95%, respectively, of the total shape variation between the three species (Fig.
As a diagnostic novel character, based on the relative warp visualization plot related to the positive extreme of RW1 (Fig.
The results of the MANOVA showed that there was a significant difference in the mean wing shapes of the three species of ash psyllids (Tab.
Wing size comparisons between the three species P. repens, P. securicola and P. machinosus showed significant differences (F = 13.74, P < 0.0001). Pairwise comparisons between the three species (using HSD post-hoc test, alpha = 0.01) showed that P. machinosus had a larger wing and significant differences with P. securicola, while P. repens had medium wing size and did not have differences with other species (Fig.
The results showed allometric growth among the species. Allometric slopes in the three species did not vary significantly, but there were still significant differences between shapes of the wings when size was held constant (Table
MANOVA: Wing shape differences in male versus female within P. machinosus, P. securicola, and P. repens and also between the three species. Allometry test: allometric growth (a), comparing allometric slope (b) and comparing shape in constant size (c) in male versus female within the three species and also between them.
species | MANOVA | Allometry tests | ||||||
---|---|---|---|---|---|---|---|---|
Wilks’ Lambda | Prob. | (a) Wilks Lambda |
(a) Prob. |
(b) Wilks Lambda |
(b) Prob. |
(c) Wilks Lambda |
(c) Prob. |
|
P. machinosus | 0.2756 | <0.0001 | 0.3914 | 3.982E-004** | 0.6884 | 0.4996 | 0.3284 | 3.348E-005** |
P. securicola | 0.3964 | 0.0005 | 0.3753 | 2.033E-004** | 0.7146 | 0.6191 | 0.5920 | 0.1295 |
P. repens | 0.4204 | 0.0012 | 0.4366 | 0.0021** | 0.5697 | 0.0982 | 0.4724 | 0.0084** |
between species | 0.0222 | <0.0001 | 0.5598 | 3.502E-004** | 0.6030 | 0.3785 | 0.0292 | 2.180E-037** |
1 | The vein M is closer to the vein Rs rather than Cu1a, or the cell r1 is narrower than the cell m1 above the junction of M1+2 and M3+4 (Fig. |
Psyllopsis repens Loginova |
– | The vein M is located between Rs and Cu1a, or the cell r1 and m1 have relatively the same width above the junction of M1+2 and M3+4 (Fig. |
2 |
2 | The vein M1+2 is closer to the vein M3+4 (Fig. |
Psyllopsis machinosus Loginova |
– | The vein M1+2 is located between Rs and M3+4 veins | Psyllopsis securicola Loginova |
Many systematic studies of different psyllid groups report larger females/wings and a number of species have been described with qualitatively different male and female wings; for example, the autumn morph of Pachypsylla japonica Miyatake, 1968 have darker wing-pattern which shows sexual dimorphism. This sexual pattern dimorphism was also sporadically found in Euphalerus fossiconis Brown & Hodkinson, 1988 (
In this study, wing shape differences were found when comparing the sexes in the two ash psyllids P. machinosus and P. repens, even after removing the allometric component. But in P. securicola, allometric analysis showed that the observed wing shape variation was due to size effects, i.e., when size effects were constant, there was no difference in the wing shape between the male and the female. Even though the sexual dimorphism in the wing shape has not been ever recorded in the superfamily Psylloidea, it is observed in some insects such as Chilo suppressalis (Walker) (Lep.: Pyralidae) (Zahiri, 2003), Chironomus imicola Kieffer, 1913 (Dip.: Chironomidae) (McLechlan, 1986), seven moth species of Sphingidae (
This phenomenon might be affected by nutrition, as
Different hypotheses have been developed to explain how sexual size allometry can arise.
In this study, it was found that forewings in males have smaller surface with straighter apical edges, which suggests friction reduction with air and might result in faster flight and so more efficiency in flights; this might result in finding females. On the other hand, the broader and slower flight in females may result in selecting host plants for oviposition and flying over plants. It is demonstrated that the more elongated wings in butterflies have a positive role in longer spatial movements (
The results showed that females of all psyllids studied, P. machinosus, P. securicola, and P. repens have larger wing sizes than those of the males. Sexual dimorphism in size also has not been ever recorded in the ash psyllids. The presence of larger wing size of females may be due to larger body size of the females and affected by the different reproductive role in the males and females (
In this study, some areas of the forewings were found to be more variable than others and the prepared key yields correct identification in all studied specimens, which suggests that the wing shape can be useful for identification. The results of GMA suggested that the three species can be discriminated with a high probability of accuracy based on their forewing shapes. Despite the high similarity between the three species, there are some differences in the coordinates of the veins that is useful in their discrimination. The differences are mainly placed in Landmarks 1, 2, 3 and 8, which are related to the veins Rs, M1+2, M3+4, and M, respectively. Based on the results, the obtained characteristics can be used as diagnostic characters to discriminate the three species studied. The other main diagnostic characteristics for the three species are related to the male and female terminalia and also some markings on the thorax, as in P. repens they have an anterior lobe and a dorsal incision on the paramere (in profile view) (
Little is known about the discrimination of psyllid species and populations using geometric and traditional morphometric methods. In previous studies, the geographic populations of the Asian citrus psyllid (ACP), Diaphorina citri Kuwayama, 1908, was investigated by geometric morphometric analyses (
The above-mentioned characteristics presented in this research can separate the three species studied; the identification of other species is certainly possible especially on the basis of male genitalia. Considering the importance of identification of species and its importance in pest management programs, morphometric studies with all ash psyllid species are suggested.
Financial support (number 95/1826) by the Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran, is gratefully acknowledged. We thank Professor Sassan Asgari (University of Queensland, Australia) for the valuable suggestions. We are grateful to Professor F. James Rohlf (State University of New York) and an anonymous reviewer for their constructive comments on the manuscript.