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1 July 2010 Grasshopper Systematics: Past, Present and Future
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Abstract

For the past 250 y, tremendous advances have been made in the field of grasshopper systematics. There have been several breakthroughs that have pushed the field forward, and behind these breakthroughs were numerous visionary taxonomists. This article is a celebration of those taxonomists and their achievements. In this review, I provide a general overview of the field and describe major advances that have shaped our understanding of grasshopper systematics. Specifically, I review the pattern of species description in Acridomorpha (Orthoptera: Caelifera) since Linnaeus, and highlight the achievements of important taxonomists. Finally, I end with some of the problems that we grasshopper taxonomists are facing today and challenge the field as a whole to move forward.

What is Acridomorpha?

The classification of Caelifera has a convoluted history (Dirsh 1961, 1975, Kevan 1976, Key 1976a). It is beyond the scope of this paper to review all the classification schemes proposed by various authors, and a concise summary can be found in Flook & Rowell (1997a: 89–91). Based on the latest classification scheme adopted by the Orthoptera Species File Online (Eades & Otte 2009), the orthopteran suborder Caelifera consists of two infraorders Tridactylidea and Acrididea. Tridactylidea contains a single extant superfamily Tridactyloidea, which consists of three families: Cylindrachetidae, Ripipterygidae and Tridactylidae. Acrididea consists of seven extant superfamilies: Acridoidea, Eumastacoidea, Pneumoroidea, Pyrgomorphoidea, Tanaoceroidea, Trigonopterygoidea and Tetrigoidea. The first six superfamilies are grasshopper-like in morphology and therefore grouped in a monophyletic superfamily group Acridomorpha. Tetrigoidea contains a single family Tetrigidae. The focus of this paper is on Acridomorpha, which contains about 24 families as a whole (Fig. 1).

Acridoidea is the largest superfamily within Orthoptera and contains about 11 extant families and about 7680 species, defined by the morphology of the male phallic complex and the lack of basioccipital slit, among other characters (Roberts 1941, Amédégnato 1974, Kevan 1982).

Most species in this group are familar and easy to recognize as typical grasshoppers. Eumastacoidea consists of about 8 extant families and about 1269 species, commonly known as the monkey grasshoppers. This group is defined by antennal tubercles and no auditory organ (Flook & Rowell 1997a).

A recent molecular phylogenetic study (Matt et al. 2008) suggests a possibility of the stick insect-like Proscopiidae being its own superfamily (Proscopioidea), sister to Eumastacoidea, because the family was never placed within any of the existing branches of Eumastacoidea. However, Proscopiidae has always been shown to have a close affinity to Eumastacoidea (Roberts 1941, Blackith & Blackith 1968, Dirsh 1975) and therefore I tentatively include it in this superfamily.

Pyrgomorphoidea contains some of the most colorful grasshopper species and consists of a single family, Pyrgomorphidae, having about 476 species, characterized by the presence of a groove in the fastigium (Kevan & Akbar 1964).

The remaining three superfamilies are small in number, highly unusual and mostly endemic. Pneumoroidea contains one family, Pneumoridae, and 17 species, mostly found in South Africa, and is known for its unique femoro-abdominal stridulatory mechanism (Dirsh 1965). Males have a swollen abdomen that can amplify their calls for a long distance signal (van Staaden & Römer 1997) and they are commonly known as bladder grasshoppers. Tanaoceroidea contains one family and 3 known species endemic to the southwestern U.S. and is characterized by extremely long antennae and a rudimentary male phallic complex (Rehn 1948, Dirsh 1975).

Finally, Trigonopterygoidea consists of two rather divergent families, Trigonopterygidae and Xyronotidae. The former is endemic to the Southeast Asia and contains about 16 species and is characterized by reversed male genitalia and foliaceous tegmina (Dirsh 1952, 1975). The latter contains four species endemic to central Mexico and can be characterized by rudimentary male genitalia and a stridulatory ridge on third abdominal tergites (Dirsh 1955). These two families form a monophyletic group based on molecular phylogeny (Flook et al. 2000).

Major advances in grasshopper systematics

The field of grasshopper systematics has been shaped by numerous taxonomists who spent their lifetimes documenting biodiversity and understanding the relationships among lineages. I consider that three major breakthroughs have been particularly crucial in propelling the field forward. They are the use of male genitalia in taxonomy, the use of molecular characters in resolving higher-level relationships, and the development of the Orthoptera Species File. Below I review and elaborate on each topic.

Male genitalia.— In insect systematics, male genitalia are arguably the most important of taxonomic characters. Their utility for species identification as well as higher-level classification has been shown in most groups of insects (Tuxen 1970). Species-specificity of male genitalia is often considered to be one of the most general trends in biology (Eberhard 1985).

Fig. 1.

Representatives of superfamilies within Acridomorpha. a, Chondracris rosea (De Geer, 1773) [Acrididae]; b, Prionolopha senata (Linnaeus, 1758) [Romaleidae]; c, Pamphagus elephas (Linnaeus, 1758) [Pamphagidae]; d, Erucius bifasciatus Stål, 1877 [Chorotypidae]; e, Apioscelis bulbosa (Scudder, 1869) [Proscopiidae]; f, Physemacris variolosa (Linnaeus, 1758) [Pneumoridae]; g, Dictyophorus spumans (Thunberg, 1787) [Pyrgomorphidae]; h, Systella philippensis (Walker, 1870) [Trigonopterygidae]; i, Xyronotus aztecus Saussure, 1884 [Xyronotidae]; j, Tanaocerus koebelei Bruner, 1906 [Tanaoceridae].

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In Orthoptera, the taxonomic value of male phallic structures was not realized until the early 20th century; most species were being described based on coloration and external morphology, rather than internal structures. Crampton (1918), Chopard (1918) and E.M. Walker (1922) were among the first morphologists who used internal structures to infer phylogenetic relationships among orthopteroid orders. Walker's (1922) contribution was particularly valuable because he proposed homologies of different parts of male genitalia among different orders. Snodgrass (1935) published a detailed anatomical study of a grasshopper abdomen, in which he described many parts of male genitalia and then (1937) brought his understanding of male terminal structures to other orthopteroid insects.

Hubbell (1932) was the first grasshopper taxonomist to use male genitalia for species-level analysis. He discovered that the phallic structure of Melanoplus was highly species-specific even among externally similar species. Since Hubbell (1932), almost all taxonomic publications on Acrididae have included discussion and illustration of male genitalia (Dirsh 1961).

Roberts (1941) was one of the first taxonomists who realized the value of the male phallic complex in higher-level classification and divided grasshoppers into two groups, Chasmosacci and Cryptosacci, based on the form of the ejaculatory sac and associated phallic structures. He argued that male genital characters provide excellent phylogenetic signal, unlike the external morphological traits that are easily influenced by environmental variation.

Dirsh (1956) published a very detailed study of male genitalia based on 778 genera in Acridomorpha, and argued that male genitalia are the single most important character for interpreting phylogenetic relationships. He also suggested that primitive groups have simpler and less differentiated phallic structures than more advanced groups. He found that the taxonomic utility of male genitalia actually varies according to groups. For example, he found that male genitalia are mostly uniform among closely related species in Acridinae and Truxalinae. This trend was also found in Oedipodinae by Barnum (1959) who studied 123 species in 45 genera of Oedipodinae. Barnum found the amount of variation in this subfamily was small compared to other groups such as Melanoplinae, and this finding was corroborated in later work by Otte (1984).

Fig. 2.

Phylogenetic hypotheses of Acridomorpha based on male genitalia by various taxonomists.

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Kevan et al. (1969a, 1969b, 1969c, 1969d, 1972) studied the male genitalia of Pyrgomorphidae and found that the structures were very useful at all taxonomic levels. Amédégnato (1974) found male genitalia to be very useful in distinguishing different groups of the Neotropical Acridoidea and reclassified the South American grasshoppers. Descamps (1973) and Key (1976b), working on the classification of Eumastacidae and Morabidae respectively, found that male genitalia were very informative in higher-level classification within Eumastacoidea.

Based on a thorough comparative study, Amédégnato (1976) demonstrated that the male phallic complex consists of three concentric layers (epiphallic, ectophallic, and endophallic structures) and becomes progressively elaborate through the evolutionary history of Acridomorpha, with the Acridoidea representing the most advanced evolutionary genital form.

Finally, Eades (2000) presented a synthesis of classification based on male genitalia and proposed a scenario regarding the evolution of the endophallus in Acridomorpha. He clearly demonstrated that the male phallic complex is very informative in understanding the higher-level classification of Acridomorpha and that each superfamily and many families can be characterized by the shape and position of phallic structures.

Because different taxonomists had different understanding of genital morphology, which led to quite different homology statements, the classification schemes changed continuously (Fig. 2); but this change represents increased knowledge and every subsequent proposal should be taken as a step toward understanding the phylogeny of Acridomorpha.

Molecular systematics.—Over the past few decades, an exponential growth in our ability to generate DNA sequence data has brought about a revolution in systematics. Previously unanswered questions arising from a lack of morphological characters, or convergence have been effectively addressed using molecular characters. Of course, molecular characters have many intrinsic problems that can complicate inferences, but it is more than fair to say that grasshopper systematics has benefited from this revolution and our understanding of the phylogenetic relationships within Acridomorpha has advanced tremendously. An excellent review by Chapco (1997) provides an overview of how molecular data were used in understanding the evolution of Orthoptera between 1970 and mid-1990. Since then, a number of important studies focusing on the phylogeny of Orthoptera, especially Acridomorpha, have been published.

The first breakthrough in grasshopper molecular systematics was the sequencing of the complete mitochondrial genome (mtgenome) of the migratory locust, Locusta migratoria by Flook et al. (1995). At that time, complete mtgenome sequences of insects were available only from four species (3 dipteran and 1 hymenopteran) and the findings of Flook et al. therefore represented the first nonholome-tabolous insect mtgenome and provided a valuable resource for comparative genomics.

Building upon these findings, Paul Flook and Hugh Rowell spearheaded grasshopper molecular systematic research for the next 10 years. They presented the first molecular phylogeny of Orthoptera (Flook & Rowell 1997b) and a more complete phylogeny of Caelifera (Flook & Rowell 1997a, Rowell & Flook 1998) based on mitochondrial ribosomal RNA genes (16S and 12S). They also explored the phylogenetic utility of nuclear ribosomal gene (18S) in resolving orthopteran phylogeny (Flook & Rowell 1998). Combining both mitochondrial and nuclear ribosomal genes, they presented the most comprehensive molecular phylogeny of Orthoptera to date (Flook et al. 1999). Their sampling (31 orthopteran ingroup and three ribosomal genes) was very small by today's standards, but it was a state-of-art study at the time of publication. Using the same markers, they published a series of taxon-specific phylogenies on Pneumoroidea (Flook et al. 2000), a grasshopper subfamily Proctolabinae (Rowell & Flook 2004), and Eumastacoidea (Matt et al. 2008). Their findings and previous understanding of morphology collectively form a basis for our current classification of Acridomorpha.

In Canada, William Chapco and his colleagues focused on understanding the phylogeny of a grasshopper subfamily Melanoplinae, using mitochondrial genes and published a series of papers (Chapco 1997; Chapco et al. 1997; Chapco et al. 1999; Chapco et al. 2001; Chapco & Litzenberger 2002a, 2002b; Amédégnato et al. 2003; Litzenberger & Chapco 2003; Chapco & Litzenberger 2004; Chapco 2006). Chapco was successful in generating sequence data from dried museum specimens and a highlight of his work was the investigation of the phylogenetic position of the now extinct Rocky Mountain locust, Melanoplus spretus, which he sequenced using DNA from 400-year-old specimens frozen in a glacier in Wyoming (Chapco & Litzenberger 2004). He also worked on the molecular phylogenetics of other grasshopper groups including Gomphocerinae (Contreras & Chapco 2006) and Oedipodinae (Fries et al. 2007).

Besides studies by these two research groups, little work has been done to clarify the higher-level classification, except for a few isolated studies by Asian researchers (Maekawa et al. 1999, Zhang et al. 2005, Bugrov et al. 2006, Huo et al. 2007, Liu et al. 2008, Yin et al. 2008); these were often based on small-taxon and character sampling.

In 2008, Fenn et al. (2008) published a preliminary molecular phylogeny based on complete mtgenome sequences and showed that mtgenome data could help resolve relationships over a broad time scale. However, their study only included three caeliferan taxa, all Acrididae, so not much could be inferred of the relationships within Acridomorpha.

Over the past several years, there has been considerable growth in the number of complete caeliferan mtgenomes in Genbank, including six acridid subfamilies (Flook et al. 1995, Fenn et al. 2008, Liu & Huang 2008, Zhang & Huang 2008, Ma et al. 2009) and one pyrgomorphid (Ding et al. 2007), and this number is expected to increase. Soon it will be possible to test the previous phylogenetic hypotheses using much larger taxon and character sampling, which may challenge the currently accepted classification scheme.

Since this paper focuses on higher-level systematics of Acridomorpha, I do not review any of the population-level studies. However, one research program deserves particular mention. Also working on the genus Melanoplus, Lacey Knowles studied the effect of the Pleistocene glaciations on speciation in a phylogeographic framework (Knowles 2000, 2001). She used a variety of molecular markers, including mitochondrial loci (Knowles 2000), AFLP (Knowles & Richards 2005), and single-copy nuclear polymorphic sequences (Carstens & Knowles 2006), to estimate phylogeny using population genetic approaches. Currently, Knowles is the leading figure in the field of statistical phylogeography, a demographic inference that takes into account the stochasticity of genetic processes (Knowles 2004, 2009).

While molecular data have clearly enriched our understanding of grasshopper systematics, it is important to understand that they are just another source of characters that can be affected by past evolutionary phenomena, phenomena which may cause incorrect phylogenetic inferences. It is beyond the scope of this paper to review all the possible issues of molecular characters, but it should be emphasized that a thorough and careful analysis of molecular characters is imperative in molecular systematics, because these characters can be easily affected by base compositional heterogeneity (Lake 1994, Lockhart et al. 1994, Galtier & Gouy 1995, Jermiin et al. 2004), among-site rate variation (Yang 1996, Felsenstein 2001, Mayrose et al. 2005), and heterotachy (Kolaczkowski & Thorton 2004, Philippe et al. 2005).

Grasshoppers are peculiar among animals in having some of the largest known nuclear genomes: 5950–20600 Mb (Bensasson et al. 2001a). To give perspective, most insect genomes are between 98 and 8900 Mb in size and the human genome is about 3400 Mb. It is hypothesized that a major proportion of the grasshopper genome is noncoding (Bensasson et al. 2001b). At the same time, grasshoppers are known to harbor the largest amount of nuclear mitochondrial pseudogenes (numts), which are nonfunctional fragments of mtDNA integrated into the nuclear genome (Lopez et al. 1994). These two observations led to a hypothesis that a large nuclear genome size is correlated with an increased number of numts, because fragments of mtDNA keep on accumulating in the noncoding region of the nuclear genome (Bensasson et al. 2000).

The first case of numts in Metazoa was reported from Locusta migratoria (Gellissen et al. 1983), in which a copy of a mitochondrial ribosomal RNA gene was found in the nuclear genome. Since then, grasshoppers have become model organisms in studying the evolution of numts (Zhang & Hewitt 1996a, 1996b; Bensasson et al. 2000; Bensasson et al. 2001b; Sword et al. 2007; Song et al. 2008).

The presence of numts poses a serious problem in PCR-based mitochondrial systematics. One of the main reasons why mtDNA has been so widely used is the ease of generating sequence data using conserved primers (Folmer et al. 1994, Simon et al. 1994, Simon et al. 2006). However, studies have consistently shown that numts are very easy to co-amplify with the orthologous mtDNA, using conserved primers (Collura & Stewart 1995, Zhang & Hewitt 1996b, Sorenson & Quinn 1998, Bensasson et al. 2001a, Benesh et al. 2006, Song et al. 2008). It is also possible to preferentially amplify numts if the nuclear integration of numts was an ancient and sufficient sequence divergence accumulated in the orthologous mtDNA (Bensasson et al. 2001a, Song et al. 2008). In 2008, I empirically showed that the coamplification of numts can lead to incorrect inferences in DNA barcoding studies (Song et al. 2008), and this finding is applicable to other types of molecular studies utilizing mtDNA as well. Therefore, it is always important to control against numts when using mtDNA as a phylogenetically informative marker and this is especially true for Acridomorpha.

Orthoptera Species File.—Perhaps the single most important milestone in grasshopper systematics (and in orthopteran systematics in general) is the development of the Orthoptera Species File Online. This concept, a collection of all taxonomic information for a single taxonomic group, was the brainchild of Daniel Otte. Otte published the first paper volume of OSF in 1994 to cover Grylloidea and subsequently a total of eight volumes to cover all Orthoptera were published by 2000. In 1997, Otte and Piotr Naskrecki developed the first online version of the OSF and in 2001 David Eades joined and further developed it using a relational database, which ultimately led to the current version of the OSF. An excellent summary on the history of the OSF can be found in the OSF website.

The OSF online contains complete synonymic and taxonomic information, citations and references, images and sound recordings, maps, specimen collecting records and identification keys. As of December 2009, the OSF online contains full information on 29,464 valid species, 41,425 scientific names, 160,586 citations to 12,333 references, 65,764 images, 188 sound recordings, 74,111 specimen records, and keys to 2,867 taxa. The OSF online uses a powerful relational model database server (Microsoft SQL Server) and most of the programming is done in Visual Basic. It extensively implements the TDWG geographic classification and the Bishop Museum system for specimen depositories. It is also capable of allowing others to import hierarchy and nomenclatural data. The contents are continuously being updated as new taxonomic studies are published. Another initiative developed from the OSF online was the Species File Software, which serves as a foundation for taxonomic database development for researchers who want to create their own taxonomic databases. So far, researchers working on other taxonomic groups, such as Plecoptera, Blattodea, Mantodea, Phasmida, Aphidomorpha, Psocodea, and Coreoidea, are extensively using the software.

Fig. 3.

A trend in species description in Acridomorpha for the last 250 years. y-axis shows the number of valid species described and x-axis shows the year of species description.

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One of the exciting features of the current version of the OSF online is the ability to generate a subset of a species file for the private use of someone working on a taxonomic revision. This gives a greater flexibility to the taxonomist who can make sure of the most up-to-date taxonomic and synonymic information and utilize many available multimedia tools such as high-resolution digital images and interactive maps of species distribution. Once the taxonomic work is published, this private copy can be merged back into the OSF online and becomes available to the public immediately. I expect to see many taxonomists utilizing this feature soon. There is no taxonomic database quite like the OSF online in terms of its breadth, capacity and interactivity, and it sets itself as a benchmark for excellence.

Trends in grasshopper systematics for the last 250 years

Since Linnaeus described Gryllus (Acrida) tunitus [= Acrida turrita] along with 26 other grasshopper species in the 10th edition of Systema Naturae in 1785, more than 9400 valid species of grasshoppers have been described by numerous taxonomists. Who were these taxonomists and what was the pattern of species description during the last 250 years? Taxonomy is a unique field of science in which one needs to completely evaluate all past works, both bad and good, since first description. Therefore, it is important to know how the field of grasshopper systematics has been shaped and by which taxonomists.

In orderto address this, I performed a complex search on the OSF online, first by constraining the scope of search to valid names only in Acridomorpha, by the year of publication using the “between” option so that species described per decades can be counted, and by specifying the rank to only include species. The search found a total of 9443 valid species of Acridomorpha described between 1785 and 2009 and the results are shown as a graph in Fig. 3. The overall trend in species description can be described as a slow start and a rapid increase, followed by a sharp decline.

Naturalists in the 18th century, such as Linnaeus, Fabricius, and Thunberg, were beginning to realize the diversity of organisms in nature, but mostly relied on specimens brought back by explorers. Only a small number of species were described by the end of 18th century and the descriptions were mostly superficial. The 19th century was a period of exponential growth in number of species described. Taxonomists affiliated with museums began to develop insect collections based on the specimens collected by explorers in the European colonies, as well as the specimens collected by the taxonomists themselves. The early taxonomists were specialists of insects and described species belonging to many different insect orders, but some focused on Orthoptera more than others. Among the notable taxonomists of 19th century were Swiss entomologists Henri Louis Frédéric de Saussure and Carl Brunner von Wattenwyl, a Spanish entomologist Ignacio Bolívar, a Swedish entomologist Carl Stål, an Italian entomologist Ermanno Giglio-Tos, and American entomologists Samuel Hubbard Scudder and Lawrence Bruner. By the end of the 19th century, over 2000 valid species of Acridomorpha (or over 3100 names, which were later synonymized) were described.

Table 1.

A list of taxonomists who have significantly contributed to the field of grasshopper systematics over the last 250 y. For each information is given on the number of valid species described, active publication dates, and the region of interest. The region of interest follows the scheme used by the OSF. Besides the obvious categories such as Africa and Europe, North America includes the LISA., Canada, Mexico, and subarctic America; South America includes the whole of Central America except Mexico, the whole of South America, and the Caribbean; Temperate Asia includes the Arabian Peninsula, Caucasus, China, Mongolia, Russia and Siberia; Tropical Asia includes the Indian Subcontinent, Indo-China, Malasia and Papuasia; and Australasia includes Australia and New Zealand. The data presented here are up-to-date as of December 2009.

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Continued

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The 20th century was a time of specialization and systematic exploration of fauna and the majority of our taxonomic knowledge on Acridomorpha comes from the taxonomists of this period. These taxonomists began to specialize on more narrow taxonomic groups (such as Acrididae, ratherthan Orthoptera) and on specific geographic regions. Therefore it is possible to name several taxonomists who were influential in describing grasshopper species from each continent. James A. G. Rehn, Morgan Hebard, H. Radclyffe Roberts, and Daniel Otte, all associated with the Academy of Natural Sciences at Philadelphia, significantly contributed to our understanding of the Nearctic grasshopper fauna mostly from North America.

These taxonomists also worked extensively on the Neotropic fauna, but there are a goodly number of taxonomists who worked exclusively on Neotropic grasshoppers. In particular, Marius Descamps, Ricardo A. Ronderos, Carlos S. Carboneil, Christiane Amé dégnato, C. Hugh Fraser Rowell, Maria Marta Cigliano, and Alba Bentos-Pereira all contributed significantly to our understanding of the grasshoppers in this region, especially in the latter half of the 20th century. Among them, Descamps stands out as the most prolific taxonomist, describing over 1000 species belonging to Acridomorpha during his tenure at the Muséum National d'Histoire Naturelle in France.

African grasshopper fauna was studied by many taxonomists already mentioned, as well as other European taxonomists, importantly, Yngve Sjöstedt, Sir Boris P. Uvarov, Willy Ramme, Vitaly M. Dirsh, D. Keith McE. Kevan, and Nicholas D. Jago. Uvarov's two-volume book Grasshopper and Locusts published in 1966 and 1977 is still considered one of the best syntheses of research on Acridomorpha, and Dirsh's comprehensive taxonomic review, The African Genera of Acridoidea, is the most useful resource on the taxonomy of African grasshoppers.

Temperate Asia was studied by Russian taxonomists Grigory Y. Bei-Bienko and Leo L. Mishchenko, and Chinese taxonomists Zhemin Zheng and Xiangchu Yin. Particularly, the two-volume book, Locusts and Grasshoppers of the U.S.S.R. and Adjacent Countries, co-authored by Bei-Bienko and Mishchenko, provides a comprehensive review on grasshoppers in temperate Asia. Tropical Asia received relatively little attention by comparison and was partly studied by Sjöstedt, Uvarov, Ramme, Candido Bolivar, Cornells J. M. Willemse and Fer M. H. Willemse, Kevan, Descamps, Sigfrid Ingrisch, and Sergei Y. Storozhenko. Australia was originally studied by Sjöstedt and Rehn, but most of what we know came from a life-long study by Kenneth H. L. Key at the CSIRO, Australian National Insect Collection. Finally, European grasshoppers have been described by many taxonomists already mentioned above. Complete data on important grasshopper taxonomists are presented in Table 1.

Unfortunately, however, the pattern of species description turns sharply in an opposite direction near the end of the 20th century. The decline does not mean we have described every single grasshopper species in the world, given the fact that only about 10% of the world's biodiversity has been described (Wheeler & Cracraft 1996). Rather, it represents a lack of taxonomic expertise to continue the enormous task of identifying and describing biodiversity; I refer to this here as the ‘taxonomic impediment’. When examined in more depth, by different geographic regions, it is clear that the sharp decline is ubiquitous across all continents (Fig. 4).

Taxonomic impediments and the need for biodiversity

We are presently living in an age of biodiversity crisis. Species are rapidly going extinct due to destruction of habitat, introduced exotic species, pollution, and climate change (Wilson 1992). At the same time, there is an enormous shortage of taxonomists who can identify and describe species (Wheeler 2004). The loss of biodiversity coupled with the taxonomic impediment is one of the most challenging issues we biologists face today.

It is a serious issue for all taxonomic groups, but the prospect is particularly bleak for the field of grasshopper systematics. Linlike the glorious days of the 20th century, when numerous taxonomists debated taxonomic concepts and classifications, there are now only a handful of active grasshopper specialists around the world, many of whom are retired or near retirement.

For other major groups of insects, there are research programs that systematically train young students in taxonomy (such as the U.S. National Science Foundation-sponsored PEET program), but no such program is yet available for grasshoppers. Globally, it has become very difficult to secure funding for basic descriptive taxonomy. This coincides with the proliferation of molecular systematics and with fewer students being trained in morphology. The fact that training in taxonomy takes a much longer time than training in molecular studies and that taxonomic studies are often only publishable in taxon-specific journals with low impact factors, probably contributes to the decline of descriptive taxonomy as well. It also has to do with economic rationalisms and changing directions and attitudes of universities and government agencies. It is therefore extremely urgent to rejuvenate grasshopper systematics by training more students through creative and innovative approaches.

Fig. 4.

Trends in species description in Acridomorpha examined according to different geographic regions.

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Although taxonomists have described more than 9400 valid species of Acridomorpha from all corners of the world, there is still great need for exploration. To illustrate this point more clearly, I performed a complex search using the OSF online, first by constraining the scope of search to valid names only in Acridomorpha and then by specifying the locality down to geographic level 3 (country). The result is shown graphically on the map of the world, coded by how well-studied each fauna is (Fig. 5).

Most of the regions, Nearctic, Neotropic and Palearctic, as well as temperate Asia (except China) and southern Africa, have been extensively studied and we have a good understanding of what grasshopper species occur in these regions. In Central America, however, we have little understanding of the grasshopper fauna in Guatemala, Belize, El Salvador, Honduras, and Nicaragua. The Hispaniola fauna has recently received much attention by Daniel Perez-Gelabert and there are still more species to discover. Some parts of South America still need to be explored despite concentrated efforts by a number of taxonomists including Descamps, Ronderos, Carbonell, Amédégnato, Cigliano, and Bentos-Pereira. Specifically, Venezuela, Guyana, Surinam, Bolivia and Chile deserve to be explored more in depth.

Africa has been studied by numerous taxonomists over the last 250 y, but western Tropical Africa still remains one of the least studied fauna. Only the orthopteran fauna of East Africa, especially near Mt Kilimanjaro has been systematically studied by Claudia Hemp.

India is also poorly studied, and recently it has become particularly challenging to work on the Indian fauna due to logistical and political problems.

China presents a different challenge. Two leading Chinese taxonomists, Zheng and Yin, and their numerous students have described a large number of species from different parts of China, but unfortunately they have adopted a taxonomic scheme of their own (Yin 1984, Zheng & Lian 1988) which elevated some tribes and subfamilies to families. For example, Chinese authors recognize “Acrypteridae” as a separate family which is a junior synonym of the gomphocerine tribe Arcypterini and “Hieroglyphinae” as a separate subfamily of “Catantopidae”, which is a junior synonym of hemiacridine tribe Hieroglyphini. Hundreds of species described from China underthe Chinese classification scheme will need to be reclassified under a phylogenetically sound classification system and this error is being recognized by the Chinese researchers themselves (Huo et al. 2007).

Southeast Asia and the islands in the Central Indo-Pacific are uncharted territories for grasshopper taxonomy. Early taxonomists such as Sjöstedt and Willemse provided a basic foundation for future studies, but the fauna has never been systematically explored. Virtually nothing is known about the grasshopper fauna of countries like Vietnam, Laos, and Cambodia and these places need desperately to be explored.

Finally, Australia presents yet another problem. Of some 225 identified genera of grasshoppers, of which 85 are yet to be described, 93% are endemic to Australia (Key 1992). Although Australia harbors only three Acridomorpha families (Pyrgomorphidae, Morabidae, and Acrididae), these (especially Catantopinae) have undergone explosive radiation, giving rise to a current high diversity of Australian grasshoppers. Although Key's lifelong investigation tremendously advanced our knowledge of the Australian fauna, there are still numerous species and genera to be described and this is particularly evident in the latest field guide on the Australian grasshoppers A Guide to Australian Grasshoppers and Locusts by Rentz et al. (2003) which included numerous unnamed species and genera.

Fig. 5.

The current status of taxonomic knowledge in grasshopper systematics in terms of countries explored. White color represents a country that is reasonably well-studied, light gray represents a country where some work has been done but is still needed to be explored, dark gray represents a country that is poorly explored, and black represents a country that has not been systematically explored at all.

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Biodiversity exploration is not a thing of the past, but the way of the future. There are still many regions of the world that need to be explored and there are still many, many grasshoppers to describe. A well-planned biodiversity survey can result in an enormous increase in knowledge. For example, a comprehensive survey of the Neotropical grasshoppers by the Muséum National d'Histoire Naturelle in the 1970s, based on a series of expeditions to Colombia, French Guiana, Peru and Brazil, led to a realization that an amazing diversity of highly specialized grasshoppers dwells in canopies. The result was the publication of an excellent taxonomic study by Amedegnato and Descamps (1979) which revealed the diversity and convergence occuring in dendrophilous grasshoppers. Compared to the 1970s, there are many more tools and technological advances available for exploratory studies and it is imperative to take advantage of these resources to understand the true diversity of grasshoppers.

A challenge

Over the last 250 y, taxonomists in the field of grasshopper systematics have created a rich legacy upon which future generations can build. It is unfortunate that the field today is suffering from the impediment to taxonomy, but it is not too late to begin to rejuvenate and revitalize grasshopper systematics.

The most important area of improvement is the recruitment of young students to taxonomy. Working grasshopper taxonomists around the world need to collaborate and share resources in order to pass on their enormous body of knowledge to the next generation. Grasshoppers represent a wonderful system to address all sorts of interesting evolutionary questions, and it is certainly possible to attract enthusiastic students to grasshopper systematics, rather than losing them to the already saturated fields of major holometabolous insects.

Another area of encouragement is to realize that taxonomy is evolving. The development of technology in digital imaging, data-basing, and cyberinfrastructure has merged with taxonomy to result in what is commonly referred to as cybertaxonomy (Wheeler 2004). The goal of cybertaxonomy is to explore and describe biodiversity rapidly and effectively, using these technological advances and so to remove the impediments to taxonomy. In this sense, grasshopper taxonomists are in a very good position because of the OSF online, which is capable of performing all the tasks related to conducting a solid cybertaxonomic study. To move forward, the field of grasshopper systematics as a whole needs to adapt to the changing environment of taxonomy and to become a leader in exploring biodiversity.

Acknowledgements

This paper is based on a presentation of the same title given at the Dan Otte Symposium held at the University of Lethbridge in June 2009. Bill Cade encouraged me to participate in the symposium in honoring Dan Otte and several people there suggested it would be informative to publish this presentation. David Eades kindly wrote a script to easily calculate statistics in the OSF online and provided details on its inner workings. David Rentz, David Eades and one anonymous reviewer provided valuable comments on the earlier version of this paper. This work is supported by the U.S. NSF grant DEB-081692.

References

  1. C. Amédégnato 1974. Les genres d'acridiens neotropicaux, leur classification par familles, sous-familles et tribus. Acrida 3: 193–203. Google Scholar

  2. C. Amédégnato 1976. Structure et évolution des genitalia chez les Acrididae et familles apparentées. Acrida 5: 1–15. Google Scholar

  3. C. Amédégnato , W. Chapco , G. Litzenberger 2003. Out of South America? Additional evidence for a southern origin of melanopline grasshoppers. Molecular Phylogenetics and Evolution 29: 115–119. Google Scholar

  4. C. Amédégnato , M. Descamps 1979. Diagnoses génériques et affinitiés phylétiques d'Acridoidea néotropicaux récoltés par de Dr Campos Seabra et M. Descamps (Orthoptera). Annales de la Société Entomologique de France 15: 423–487. Google Scholar

  5. A.H. Barnum 1959. The phallic complex in the Oedipodinae (Orthoptera: Acrididae). Entomology, Iowa State College: 220. Google Scholar

  6. D.P. Benesh , T. Hasu , L.R. Suomalainen , E.T. Valtonen , M. Tiirola 2006. Reliability of mitochondrial DNA in an acanthocephalan: the problem of pseudogenes. International Journal for Parasitology 36: 247–254. Google Scholar

  7. D. Bensasson , D.-X. Zhang , D.L. Hartl , G.M. Hewitt 2001a. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology and Evolution 16: 314–321. Google Scholar

  8. D. Bensasson , D.A. Petrov , D.-X. Zhang , D.L. Hartl , G.M. Hewitt , 2001b. Genomic gigantism: DNA loss is slow in mountain grasshoppers. Molecular Biology and Evolution 18: 246–253. Google Scholar

  9. D. Bensasson , D.-X. Zhang , G.M. Hewitt 2000. Frequent assimilation of mitochondrial DNA by grasshopper nuclear genomes. Molecular Biology and Evolution 17: 406–415. Google Scholar

  10. R.E. Blackith , R.M. Blackith 1968, A numerical taxonomy of orthopteroid insects. Australian Journal of Zoology 16: 111–131. Google Scholar

  11. A. Bugrov , O. Novikova , V. Mayorov , L. Adkison , A. Blinov 2006. Molecular phylogeny of Palaeartic genera of Gomphocerinae grasshoppers (Orthoptera, Acrididae). Systematic Entomology 31: 362–368. Google Scholar

  12. B.C. Carstens , L.L. Knowles 2006. Variable nuclear markers for Melanoplus oregonensis identified from the screening of a genomic library. Molecular Ecology Notes 6: 683–685. Google Scholar

  13. W. Chapco 1997. Molecular evolutionary genetics in orthopteroid insects, pp. 337–354. In: S.K. Gangwere , M.C. Muralirangan , M. Muralirangan (Eds) The Bionomics of Grasshoppers, Katydids and Their Kin. Oxon, UK, CAB International. Google Scholar

  14. W. Chapco 2006. A note on the phylogenetic position of Duartettix montanus within the subfamily Melanoplinae. Journal of Orthoptera Research 15: 59–63. Google Scholar

  15. W. Chapco , W.R. Kuperus , G. Litzenberger 1999. Molecular phylogeny of Melanopline grasshoppers (Orthoptera: Acrididae): The genus Melanoplus. Annals of the Entomological Society of America 92: 617–623. Google Scholar

  16. W. Chapco , G. Litzenberger 2002a. A molecular phylogenetic analysis of the grasshopper genus Melanoplus Stål (Orthoptera: Acrididae) - an update. Journal of Orthoptera Research 11: 1–9. Google Scholar

  17. W. Chapco , G. Litzenberger 2002b. A molecular phylogenetic study of two relic species of melanopline grasshoppers. Genome 45: 313–318. Google Scholar

  18. W. Chapco , G. Litzenberger 2004. A DNA investigation into the mysterious disappearance of the Rocky Mountain grasshopper, mega-pest of the 1800s. Molecular Phylogenetics and Evolution 30: 810–814. Google Scholar

  19. W. Chapco , G. Litzenberger , W.R. Kuperus 2001. A molecular biogeographic analysis of the relationship between North American melanoploid grasshoppers and their Eurasian and South American relatives. Molecular Phylogenetics and Evolution 18: 460-466. Google Scholar

  20. W. Chapco , R.K.B. Martel , W.R. Kuperus 1997. Molecular phylogeny of North American band-winged grasshoppers (Orthoptera: Acrididae). Annals of the Entomological Society of America 90: 555-562. Google Scholar

  21. L. Chopard 1918. Note préliminaire sur la conformation de l'organe copulateur des Orthoptères. Bulletin de la Societe Zoologique de France 43: 59-67. Google Scholar

  22. R.V. Collura , C.B. Stewart 1995. Insertions and duplications of mtDNA in the nuclear genomes of Old World monkeys and hominoids. Nature 378: 485–489. Google Scholar

  23. D. Contreras , W. Chapco 2006. Molecular phylogenetic evidence for multiple dispersal events in gomphocerine grasshoppers. Journal of Orthoptera Research 15: 91–98. Google Scholar

  24. G.C. Crampton 1918. A phylogenetic study of the terminal abdominal structures and genitalia of male Apterygota, Ephemerids, Odonata, Plecoptera, Neuroptera, Orthoptera, and their allies. Bulletin of the Brooklyn Entomological Society 13: 49–68. Google Scholar

  25. M. Descamps 1973. Révision des Eumastacoidea (Orthoptera) aux échelons des familles et des sous-familles (Genitalia, répartition, phylogénie). Acrida 2: 161–298. Google Scholar

  26. F.-M. Ding , H.-W. Shi , Y. Huang 2007. Complete mitochondrial genome and secondary structures of lrRNA and srRNA of Atractomorpha sinensis (Orthoptera, Pyrgomorphidae). Zoological Research 29: 580–588. Google Scholar

  27. V.M. Dirsh 1952. The restoration of the subfamily Trigonopteryginae Walker (Orthoptera, Acrididae). Annals and Magazine of Natural History 5: 82–84. Google Scholar

  28. V.M. Dirsh 1955. Tanaoceridae and Xyronotidae, two new families of Acrioidea (Orthoptera). Annals and Magazine of Natural History 8: 285–288. Google Scholar

  29. V.M. Dirsh 1956. The phallic complex in Acridoidea (Orthoptera) in relation to taxonomy. Transactions of the Royal Entomological Society of London 108: 223–356. Google Scholar

  30. V.M. Dirsh 1961. A preliminary revision of the families and subfamilies of Acridoidea (Orthoptera, Insecta). Bulletin of the British Museum (Natural History) Entomology 10: 351–419. Google Scholar

  31. V.M. Dirsh 1965. Revision of the family Pneumoridae (Orthoptera: Acridoidea). Bulletin of the British Museum (Natural History) Entomology 15: 325–396. Google Scholar

  32. V.M. Dirsh 1975. Classification of the Acridomorphoid Insects. Faringdon, Oxon, E.W. Classey Ltd. Google Scholar

  33. D.C. Eades 2000. Evolutionary relationships of phallic structures of Acridomorpha (Orthoptera). Journal of Orthopteran Research 9: 181–210. Google Scholar

  34. D.C. Eades , D. Otte 2009. Orthoptera Species File Online. Version 2.0/3.5 [10/1/2009]. < http://Orthoptera.SpeciesFile.org>. Google Scholar

  35. W.G. Eberhard 1985. Sexual selection and animal genitalia. Massachusetts, Harvard University Press. Google Scholar

  36. J. Felsenstein 2001. Taking variation of evolutionary rates between sites in account in inferring phylogenies. Journal of Molecular Evolution 53: 447–455. Google Scholar

  37. J.D. Fenn , H. Song , S.L. Cameron , M.F. Whiting 2008. A mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Molecular Phylogenetics and Evolution 49: 59–68. Google Scholar

  38. P.K. Flook , S. Klee , C.H.F. Rowell 1999. Combined molecular phylogenetic analysis of the Orthoptera (Arthropoda, Insecta) and implications for their higher systematics. Systematic Biology 48: 233–253. Google Scholar

  39. P.K. Flook , S. Klee , C.H.F. Rowell 2000. Molecular phylogenetic analysis of the Pneumoroidea (Orthoptera, Caelifera): Molecular data resolve morphological character conflicts in the basal Acridomorpha. Molecular Phylogenetics and Evolution 15: 345–354. Google Scholar

  40. P.K. Flook , C.H.F. Rowell 1997a. The phylogeny of the Caelifera (Insecta, Orthoptera) as deduced from mtrRNA gene sequences. Molecular Phylogenetics and Evolution 8: 89–103. Google Scholar

  41. P.K. Flook , C.H.F. Rowell 1997b. The effectiveness of mitochondrial rRNA gene sequences for the reconstructions of the phylogeny of an insect order (Orthoptera). Molecular Phylogenetics and Evolution 8: 177–192. Google Scholar

  42. P.K. Flook , C.H.F. Rowell 1998. Inferences about orthopteroids phylogeny and molecular evolution from small subunit nuclear ribosomal DNA sequences. Insect Molecular Biology 7: 163–178. Google Scholar

  43. P.K. Flook , C.H.F. Rowell , G. Gellissen 1995. The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome. Journal of Molecular Evolution 41: 928–941. Google Scholar

  44. O. Folmer , M. Black , W. Hoeh , R. Lutz , R. Vrijenhoek 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3: 294–299. Google Scholar

  45. M. Fries , W. Chapco , D. Contreras 2007. A molecular phylogenetic analysis of the Oedipodinae and their intercontinental relationships. Journal of Orthoptera Research 16: 115–125. Google Scholar

  46. N. Galtier , M. Gouy 1995. Inferring phylogenies from DNA sequences of unequal base compositions. Proceedings of the National Academy of Sciences, USA 92: 11317–11321. Google Scholar

  47. G. Gellissen , J.Y. Bradfield , B.N. White , G.R. Wyatt 1983. Mitochondrial DNA sequences in the nuclear genome of a locust. Nature 301: 631–634. Google Scholar

  48. T.H. Hubbell 1932. A revision of the Puer group of the North American genus Melanoplus, with remarks on the taxonomic value of the concealed male genitalia in the Cyrtacanthacridinae (Orthoptera, Acrididae). Miscellaneous Publications Museum of Zoology, University of Michigan 23: 1–64. Google Scholar

  49. G. Huo , G. Jiang , Z. Sun , D. Liu , Y. Zhang , L. Lu 2007. Phylogenetic reconstruction of the family Acrypteridae (Orthoptera: Acridoidea) based on mitochondrial cytochrome b gene. Journal of Genetics and Genomics 34: 294–306. Google Scholar

  50. L. Jermiin , S.Y. Ho , F. Ababneh , J. Robinson , A.W. Larkum 2004. The biasing effect of compositional heterogeneity on phylogenetic estimates may be underestimated. Systematic Biology 53: 638–643. Google Scholar

  51. D.K.M. Kevan 1976. Book Review: Classification of the Acridomorphoid Insects. South African Journal of Science 72: 316–319. Google Scholar

  52. D.K.M Kevan . 1982. Orthoptera. Pp. 352–383. Synopsis and Classification of Living Organisms. McGraw-Hill Book Company, Inc. Google Scholar

  53. D.K.M. Kevan , S.S. Akbar 1964. The Pyrgomorphidae (Orthoptera: Acridoidea): Their systematics, tribal divisions, and distribution. Canadian Entomologist 96: 1505–1536. Google Scholar

  54. D.K.M. Kevan , S.S. Akbar , Y.-C. Chang 1969a. The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part I. General introduction. Eos 44: 165–266. Google Scholar

  55. D.K.M. Kevan , S.S. Akbar , Y.-C. Chang 1969b. The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part II. Tribes Fijipyrgini, Verduliini, Brunniellini, Psednurini, Mitricephalini, Geloiini, Sagittacridini, Gymnohippini and Malagasphenini. Eos 45: 173–228. Google Scholar

  56. D.K.M. Kevan , S.S. Akbar , Y.-C. Chang 1969c. The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part III. Tribes Chapmanacridini, Ichthiacridini, Ichthyotettigini, Orthacridini, Popoviini and Nereniini. Eos 46: 123–210. Google Scholar

  57. D.K.M. Kevan , S.S. Akbar , Y.-C. Chang 1969d. The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part IV. Tribes Desmopterini, Monistriini, Chlorizeinini, Poekilocerini and Phymateini. Eos 47: 137–234. Google Scholar

  58. D.K.M. Kevan , S.S. Akbar , Y.-C. Chang 1972. The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part V. Tribes Schulthessiini, Taphronotini, Dictyophorini, Tagastini, Pseudomorphacridini, Atractomorphini, Sphenariini and Omurini. Eos 48: 203–294. Google Scholar

  59. K.H.L. Key 1976a. Book Review: Classification of the Acridomorphoid Insects. Journal of the Australian Entomological Society 15: 152. Google Scholar

  60. K.H.L. Key 1976b. A generic and suprageneric classification of the Morabinae (Orthoptera: Eumastacidae), with description of the type species and a bibliography of the subfamily. Australian Journal of Zoology Supplementary Series 37: 1–185. Google Scholar

  61. K.H.L. Key 1992. A higher classification of the Australian Acridoidea (Orthoptera). I. General introduction and subfamily Oxyinae. Invertebrate Taxonomy 6: 547–551. Google Scholar

  62. L.L. Knowles 2000. Test of Pleistocene speciation in montane grasshoppers from the sky islands of western North America (genus Melanoplus). Evolution 54: 1337–1348. Google Scholar

  63. L.L. Knowles 2001. Genealogical portraits of speciation in montane grasshoppers (genus Melanoplus) from the sky islands of the Rocky Mountains. Proceedings of the Royal Society of London Series B 268: 319–324. Google Scholar

  64. L.L. Knowles 2004. The burgeoning field of statistical phylogeography. Journal of Evolutionary Biology 17: 1–10. Google Scholar

  65. L.L. Knowles 2009. Statistical Phylogeography. Annual Review of Ecology, Evolution, and Systematics 40: 593–612. Google Scholar

  66. L.L. Knowles , C.L. Richards 2005. Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation. Molecular Ecology 14: 4023–4032. Google Scholar

  67. B. Kolaczkowski , J.W. Thorton 2004. Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431: 980–984. Google Scholar

  68. J.A. Lake 1994. Reconstructing evolutionary trees from DNA and protein sequences: Paralinear distances. Proceedings of the National Academy of Sciences, USA 91: 1455–1459. Google Scholar

  69. G. Litzenberger , W. Chapco 2003. The North American Melanoplinae (Orthoptera: Acrididae): a molecular phylogenetic study of their origins and taxonomic relationships. Annals of the Entomological Society of America 96: 491–497. Google Scholar

  70. D.-F. Liu , Z.-M. Dong , D.-Y. Zhang , Y.-Z. Gu , P.-J. Guo , R.-H. Han , G.-F. Jiang 2008. Molecular phylogeny of the higher category of Acrididae (Orthoptera: Acridoidea). Zoological Research 29: 585–591. Google Scholar

  71. Y. Liu , Y. Huang 2008. Sequencing and analysis of complete mitochondrial genome of Chorthippus chinensis Tarb. Chinese Journal of Biochemistry and Molecular Biology 24: 329–335. Google Scholar

  72. P.J. Lockhart , M.A. Steel , M.D. Hendy , D. Penny 1994. Recovering evolutionary trees under a more realistic model of sequence. Molecular Biology and Evolution 11: 605–612. Google Scholar

  73. J.V. Lopez , N. Yuhki , R. Masuda , W. Modi , S.J. O'Brien 1994. Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution 39: 174–190. Google Scholar

  74. C. Ma , C. Liu , P. Yang , L. Kang 2009. The complete mitochondrial genomes of two band-winged grasshoppers, Gastrimargus marmaratus and Oedaleus asiaticus. BMC Genomics 10: 156. Google Scholar

  75. K. Maekawa , O. Kitade , T. Matsumoto 1999. Molecular phylogeny of orthopteroid insects based on the mitochondrial cytochrome oxidase II gene. Zoological Science 16: 175–184. Google Scholar

  76. S. Matt , P.K. Flook , C.H.F. Rowell 2008. A partial molecular phylogeny of the Eumastacoidea s. lat. (Orthoptera, Caelifera). Journal of Orthoptera Research 17: 43–55. Google Scholar

  77. I. Mayrose , N. Friedman , T. Pupko 2005. A gamma mixture model better accounts for among site rate heterogeneity. Bioinformatics 21 Suppl. 2: ii151–ii158. Google Scholar

  78. D. Otte 1984. The North American Grasshoppers Volume II. Acrididae, Oedipodinae. Cambridge, Massachusetts, Harvard University Press. Google Scholar

  79. H. Philippe , Y. Zhou , H. Brinkmann , N. Rodrigue , F. Delsuc 2005. Heterotachy and long-branch attraction in phylogenetics. BMC Evolutionary Biology 5: 50. Google Scholar

  80. J.A.G. Rehn 1948. The locust genus Tanaocerus as found in the United States, and the description of a related new genus (Orthoptera: Acrioidea). Proceedings of the Academy of Natural Sciences of Philadelphia 100: 1–22. Google Scholar

  81. D.C.F. Rentz , R.C. Lewis , Y.N. Su , M.S. Upton 2003. A Guide to Australian Grasshoppers and Locusts. Kota Kinabalu, Natural History Publications (Borneo). Google Scholar

  82. H.R. Roberts 1941. A comparative study of the subfamilies of the Acrididae (Orthoptera) primarily on the bases of their phallic structures. Proceedings of the Academy of Natural Sciences of Philadelphia 93: 201–246. Google Scholar

  83. C.H.F. Rowell , P.K. Flook 1998. Phylogeny of the Caelifera and the Orthoptera as derived from ribosomal gene sequences. Journal of Orthoptera Research 7: 147–156. Google Scholar

  84. C.H.F. Rowell , P.K. Flook 2004. A dated molecular phylogeny of the Proctolabinae (Orthoptera, Acrididae), especially the Lithoscirtae, and the evolution of their adaptive traits and present biogeography. Journal of Orthoptera Research 13: 35–56. Google Scholar

  85. C. Simon , T.R. Buckley , F. Frati , J.B. Stewart , A.T. Beckenbach 2006. Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 37: 545–579. Google Scholar

  86. C. Simon , F. Frati , A. Beckenbach , B. Crespi , H. Liu , P. Flook 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87: 651–701. Google Scholar

  87. R.E. Snodgrass 1935. The abdominal mechanisms of a grasshopper. Smithsonian Miscellaneous Collections 94: 1–89. Google Scholar

  88. R.E. Snodgrass 1937. The male genitalia of Orthopteroid insects. Smithsonian Miscellaneous Collections 96: 1–107. Google Scholar

  89. H. Song , J.E. Buhay , M.F. Whiting , K.A. Crandall 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the USA 105: 13486–13491. Google Scholar

  90. M.D. Sorenson , T.W. Quinn 1998. Numts: a challenge for avian systematics and population biology. The Auk 115: 214–221. Google Scholar

  91. G.A. Sword , L.B. Senior , J.F. Gaskin , A. Joern 2007. Double trouble for grasshopper molecular systematics: intra-individual heterogeneity of both mitochondrial 12S-valine–16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acrididae). Systematic Entomology 32: 420–428. Google Scholar

  92. S.L. Tuxen , Ed . 1970. Taxonomist's glossary of genitalia in insects. Copenhagen, Scandinavian University Press. Google Scholar

  93. M.J. van Staaden , H. Römer 1997. Sexual signaling in bladder grasshoppers: tactical design for maximizing calling range. Journal of Experimental Biology 200: 2597–2608. Google Scholar

  94. E.M. Walker 1922. The terminal structures of orthopteroid insects: a phylogenetic study. Annals of the Entomological Society of America 15: 1–76. Google Scholar

  95. Q.D. Wheeler 2004. Taxonomic triage and the poverty of phylogeny. Philosophical Transactions of the Royal Society of London Series B 359: 571–583. Google Scholar

  96. Q.D. Wheeler , J. Cracraft 1996. Taxonomic preparedness: are we ready to meet the biodiversity challenge?, pp. 435–466. In: E.O. Wilson , M. Kudla-Reaka , D. Wilson (Eds) Biodiversity II: Understanding and protecting our biological resources. Washington, DC, National Academy of Sciences Press. Google Scholar

  97. E.O. Wilson 1992. The diversity of life. Cambridge, Massachusetts, Harvard University Press. Google Scholar

  98. Z. Yang 1996. Among-site rate variation and its impact on phylogenetic analyses. Trends in Ecology & Evolution 11: 367–372. Google Scholar

  99. X.-C. Yin 1984. Grasshoppers and locusts from Qinghai-Xizang plateau of China. Beijing, China, Science Press. Google Scholar

  100. X.-C. Yin , X.-J. Li , W.-Q. Wang , H. Yin , C.-Q. Cao , B.-H. Ye , Z. Yin 2008. Phylogenetic analyses of some genera in Oedipodinae (Orthoptera: Acridoidea) based on 16S mitochondrial partial gene sequences. Insect Science 15: 471–476. Google Scholar

  101. C. Zhang , Y. Huang 2008. Complete mitochondrial genome of Oxya chinensis (Orthoptera, Acridoidea). Acta Biochimica et Biophysica Sinica 40: 7–18. Google Scholar

  102. D.-C. Zhang , X.-J. Li , W.-Q. Wang , H. Yin , Z. Yin , X.-C. Yin 2005. Molecular phylogeny of some genera of Pamphagidae (Acridoidea, Orthoptera) from China based on mitochondrial 16S rDNA sequences. Zootaxa 1103: 41–49. Google Scholar

  103. D.-X. Zhang , G.M. Hewitt 1996a. Highly conserved nuclear copies of the mitochondrial control region in the desert locust Schistocerca gregaria: some implications for population studies. Molecular Ecology 5: 295–300. Google Scholar

  104. D.-X. Zhang , G.M. Hewitt 1996b. Nuclear integrations: challenge for mitochondrial DNA markers. Trends in Ecology and Evolution 11: 247–251. Google Scholar

  105. Z.-M. Zheng , Z.-M. Lian 1988. Taxonomy of grasshoppers. Sichuan Journal of Zoology 7: 39–43.  Google Scholar

Hojun Song "Grasshopper Systematics: Past, Present and Future," Journal of Orthoptera Research 19(1), (1 July 2010). https://doi.org/10.1665/034.019.0112
Received: 9 December 2009; Accepted: 1 March 2010; Published: 1 July 2010
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