Tropical Natural History 21(1): 79–93, April 2021 ©2021 by Chulalongkorn University Taxonomic Progress and Diversity of Ichneumonoid Wasps (Hymenoptera: Ichneumonoidea) in Southeast Asia NUT SONGVORAWIT, DONALD L. J. QUICKE AND BUNTIKA AREEKUL BUTCHER Integrative Ecology Laboratory, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok 10330, THAILAND *Corresponding author. Buntika Areekul Butcher ([email protected]) Received: 25 November 2020; Accepted: 31 January 2021 ABSTRACT.– Taxonomic studies on parasitoid wasps in the superfamily Ichneumonoidea occurring in Southeast Asia (SEA) are reviewed from a historical perspective. A list of all described species in this group until the end of 2019 was compiled for each SEA country and the taxonomic effort expended in each calculated. Taxonomic effort over time differed significantly between countries, probably largely due to historical events. Involvement of local taxonomists started soon after 1900 but the proportion remained extremely low when compared to foreign experts, and although increasing markedly since 1990, remains very low. KEY WORDS: accumulation curve, Braconidae, estimation, Ichneumonidae, species richness, taxonomists, tropics rapidly increasing (Bebber et al., 2007; Schipper INTRODUCTION et al., 2008; Giam et al., 2010; Achterberg and Long, 2010). The vast majority of species Taxonomists have been finding and remain undescribed, especially in the tropics. describing new taxa for several hundred The parasitoid wasps (Hymenoptera: years before the era of Linnaeus, who Apocrita excluding most of the Aculeata) established the fundamental system of are a highly diverse group of insects nomenclature that is used universally today (Sharkey, 2007; Jones et al., 2009; Yu et al., (Ereshefsky, 2000; Winsor, 2003). The total 2012). They play key roles in terrestrial number of animal species has variously ecosystems through regulating the populations been predicted to be from 1.8 to 30 million of their hosts, predominantly other insect species, depending on the methods of species, which they ultimately and invariably estimation, while the current total number of kill (Wharton, 1993; Chen et al., 2014; Quicke, described species recorded in the Catalogue 2015). Due to their biology, parasitoid wasps of Life (CoL) in 2019 was approximately are of interest to applied scientists through their 1.8 million species (Erwin, 1982; Costello et use in biological control and integrated pest al., 2011; Mora et al., 2011; Roskov et al., management (IPM) programmes to limit 2019). New species are being discovered damage caused by insect pests both in and described in all major groups of organisms agricultural areas and in stored products every year, but although discovering new taxa (Schöller et al., 1997; Grieshop et al., 2006; in some charismatic groups, such as mammals, Venkatesan et al., 2007; Wang et al., 2014). birds and butterflies, is becoming harder, the rate of description in most other groups is 80 TROPICAL NATURAL HISTORY 21(1), APRIL 2021 The Ichneumonoidea is the largest super- et al., 2004; Giam et al., 2010; Webb et al., family in Hymenoptera in terms of described 2010). Considering to the number of ichneu- species (Chen et al., 2014). It comprises two monoid species in this region, 1,294 species extremely large families, the Braconidae of Braconidae and 710 species of Ichneu- and Ichneumonidae (Quicke, 2012, 2015; monidae have been recorded in Taxapad Chen et al., 2014), with 18,580 and 23,765 until 2012 (Yu et al., 2012), much lower described species, respectively (Roskov et than extrapolated numbers (Jones et al., 2009). al., 2019), and another small family Trachy- This indicates that taxonomic work on this petidae has been recently erected in 2020 superfamily is far from the complete and with seven species (Quicke et al., 2020). requires a great deal more taxonomic effort. However, widely quoted estimates of total Over recent years there have been a global species richness for these are several number of collaborations between western times larger, 32,000–42,000 and 60,000– and local researchers that aim to survey and 100,000, respectively (Townes et al., 1965; reinforce taxonomic studies on this region, Heinrich, 1978; Dolphin and Quicke, 2001; for example, the Thailand Inventory Group Jones et al., 2009) but even these are for Entomological Research (TIGER) project probably major underestimates (Rodrigues in Thailand (NSF, 2008). Furthermore, et al., 2013; Sharkey et al. 2021). molecular techniques have become an important Most ichneumonoids are primary para- tool for identification and classification in sitoids and attack the immature stages of various organisms, including parasitoid wasps Lepidoptera, Hymenoptera, Coleoptera and (Hebert and Gregory, 2005; Hajibabaei et Diptera, some of which are serious pests al., 2007; Smith et al., 2008, 2009; Butcher causing substantial loss of agricultural et al., 2012). productivity (Wharton, 1993; Chen et al., 2014). The species richness of a region is a Further, their role in natural ecosystems is measure of its biodiversity that can have likely to be critical in regulating populations implications for resource management as of most species of herbivores from foliage- well as conservation programmes. However, eaters to wood-borers. for many groups of organisms in SEA, Southeast Asia (SEA) is located in the taxonomic inventories are far from complete. tropics between the Pacific (in the east) and Taxonomic studies on ichneumonoids in the Indian (in the west) oceans (Sodhi et al., region began over 200 years ago, but the 2004). The region combines four biodiversity current number recorded species is still far hotspots, i.e. Indo-Burma, Sundaland, the lower than predictions (DeGeer, 1773; Jones Philippines, and Wallacea, making it one of et al., 2009; Quicke, 2012). A marked increase the most world’s species-rich areas with 20– in the rate of species description, especially 25% of the total global plant and animal in Indonesia, Malaysia and the Philippines, species (Sodhi et al., 2004; Woodruff, 2010; took place during the early 20th century Bruyn et al., 2014). However, biodiversity which coincides with a period of colonial in SEA is facing the combined major expansion (Osborne, 2016). Taxonomic effort problems of deforestation and other habitat over time differs significantly between loss due to economic development and poor countries probably due to specific historical resource management. Many species are events. After 2000, description rates and the threatened and it is probable that some will number of taxonomists involved, substantially go extinct before ever being recorded (Sodhi increased mainly with the contributions of SONGVORAWIT ET AL. — TAXONOMIC PROGRESS AND DIVERSITY OF ICHNEUMONOID WASPS 81 taxonomists in Thailand and Vietnam, e.g. country records were counted as related Butcher et al. (2012) and Achterberg and taxonomists in SEA. However, there were Long (2010). The number of local taxonomists some species that were firstly found outside is slowly increasing but is still very low when SEA, but later recorded in SEA. In those compared to the number of foreign experts. cases, author names were excluded from Here we collate all taxonomic studies of analyses. Ichneumonoidea found in SEA and compare Comparisons of taxonomic efforts taxonomic effort in the component countries. To examine taxonomic efforts in each country, discovery of new species or new country record was compared using the k- MATERIALS AND METHODS sample Anderson-Darling (AD) test, which is a nonparametric statistic for testing the Compilation of known taxa homogeneity of samples (Anderson and Southeast Asia consists of 11 countries: Darling, 1952). Cambodia was excluded Brunei, Cambodia, East Timor, Indonesia, from the analysis due to the very low Laos, Malaysia, Myanmar, the Philippines, number of species records. Statistical Singapore, Thailand and Vietnam. These are analysis was performed using the kSamples each considered separately except for Timor in R version 4.0.3 (R Core Team, 2020) island, part of which is possessed by Indonesia and part the recently independent country of East Timor, because past much RESULTS work did not specify from which part of the island material originated. However, all Known taxa published records for Timor island predate Up until the end of 2019, 27 subfamilies, the internationally recognition of East 282 genera and 1,811 species of Braconidae, Timor as an independent state in 2002. and 26 subfamilies, 273 genera and 1,119 Hence, localities of wasps found in Timor species of Ichneumonidae had been recorded island are herein treated as a part of in SEA (see details in supplementary Indonesia. materials: Tables S1 and S2 and electronic Data of ichneumonoid species and their supplement material: https://doi.org/10.5281/ distributions up until 2012 were largely zenodo.4467926). Of these, Indonesia had extracted from Taxapad (Yu et al., 2012). the highest species richness in terms of Additional literature relating to the period actual number of known species, while 2012-19 was gathered from Google, Science Singapore had the highest recorded species Direct, Scopus and Web of Science, using density per area for both families (Tables 1 search terms “[name of country] AND and 2). Cambodia had the fewest wasp Braconidae/Ichneumonidae”. The data were records with only two species of braconids then scrutinised to prevent redundancy and three species of ichneumonids. Within the such as through duplication and synonymy. Braconidae, the Braconinae had the highest Taxa not identified to species level were species diversity followed by Agathidinae, excluded. Rogadinae and Doryctinae, while for the Number of taxonomists working in SEA Ichneumonidae, the Ichneumoninae, Pimplinae Names presented in the authorship of and Cryptinae were the top species-rich binomens and authors who reported the first subfamilies (Fig. 1). 82 TROPICAL NATURAL HISTORY 21(1), APRIL 2021 TABLE 1. Number of taxa and taxonomists relating to Braconidae in SEA. BN KH ID LA MY MM PH SG TH VN SEA No. of 11 2 25 9 24 13 19 9 15 20 27 subfamilies No. of 21 2 174 26 129 37 120 19 79 80 282 genera No. of 33 2 604 40 482 54 412 27 377 261 1,811 species Density 0.00572 0.00001 0.00032 0.00017 0.00146 0.00008 0.00137 0.03721 0.00074 0.00079 0.00040 (species/km2) No. of 21 3 66 21 65 27 57 22 63 45 132 taxonomists BN = Brunei, KH = Cambodia, ID = Indonesia, LA = Laos, MY = Malaysia, MM = Myanmar, PH = the Philippines, SG = Singapore, TH = Thailand and VN = Vietnam TABLE 2. Number of taxa and taxonomists relating to Ichneumonidae in SEA. BN KH ID LA MY MM PH SG TH VN SEA No. of 5 3 21 11 19 16 15 9 17 16 26 subfamilies No. of genera 7 3 205 44 115 70 68 22 39 92 273 No. of species 42 3 656 114 296 162 175 55 97 344 1,119 Density 0.00729 0.00002 0.00034 0.00048 0.0009 0.00024 0.00058 0.07579 0.00019 0.00104 0.00025 (species/km2) 0 No. of 23 6 76 30 61 35 41 30 45 52 120 taxonomists BN = Brunei, KH = Cambodia, ID = Indonesia, LA = Laos, MY = Malaysia, MM = Myanmar, PH = the Philippines, SG = Singapore, TH = Thailand and VN = Vietnam Taxonomic studies in ichneumonoids in over 130 species from these two countries, SEA have proceeded since the 18th century while the rapid increase of ichneumonid in which the earliest described species is description post 2010 mainly reflected work ichneumonid wasp Camptotypus rugosus in on the Vietnamese fauna. 1733 (DeGeer, 1773). Rates of species Comparisons of description rates indicate description showed a marked increase during that the discovery of new species or new the 20th century. Braconid wasp species records over time differed significantly accumulation increased rapidly during the between countries for both Braconidae (AD early 1900s which largely reflects the increase = 529.6, n = 9, P < 0.001) and Ichneumonidae of descriptions of Indonesian, Malaysian and (AD = 356.2, n = 9, P < 0.001), notably Philippine taxa. Subsequently, the rate began because of work on Thai and Vietnamese declining in 1920 (Fig. 2). The rate of taxa (Tables 3 and 4). The current number description in SEA increased again starting of wasp species is presented in shaded maps around 1990 and increased abruptly from in Fig. 3 which indicated that the numbers 2010 onwards, which primarily reflects of recorded species is higher in island taxonomic effort in Thailand and Vietnam. countries than in continental countries. The SEA ichneumonid species accumu- Number of taxonomists working in SEA lation curve was similar to that of the The number of authors publishing new Braconidae except for the 1930s when there species or records of both braconid and was an abrupt increase due to taxonomic ichneumonid wasps before 1990 was work in Indonesia and Myamar, especially normally between 15 and 30 per decade, the work of Heinrich (1934) who described with a slight dip from 1931 to 1960 (Fig. 4). SONGVORAWIT ET AL. — TAXONOMIC PROGRESS AND DIVERSITY OF ICHNEUMONOID WASPS 83 FIGURE 1. Current diversity of the subfamilies of braconid and ichneumonid wasps recorded in SEA. However, the number almost doubled after DISCUSSION 1991. The number of taxonomists working with braconids was consistently higher than Several earlier studies on the relationship for ichneumonids across all years. However, between latitude and species richness local taxonomists were only involved after indicated that diversity of the family 1990 and even though their ratio compared Ichneumonidae revealed an inverse latitudinal to foreign taxonomists was always much cline, so-called anomalous diversity, in lower (1:13.5 for braconids and 1:8 for which the species richness is positively ichneumonids). 84 TROPICAL NATURAL HISTORY 21(1), APRIL 2021 FIGURE 2. Species accumulation curves of Braconidae and Ichneumonidae recorded in SEA. correlated with latitude (Owen and Owen, hypothesis, in which the proportion of 1974; Gauld, 1986; Kindlmann et al., 2007). unpalatable hosts is higher in the tropics Sime and Brower (1998) discussed the resulting in low diversity of associated various hypotheses that had put forward to wasps. However, number of ichneumonid explain anomalous diversity of ichneumonids records in SEA is still continually increasing by examining taxonomic and geographical without the sign of asymptote due to the distribution in the butterfly hosts, like increase of taxonomic efforts in this region Papilionoidea and concluded that the (Fig. 2). Therefore, it is not at all clear diversity pattern of parasitoid wasps is most whether the Ichneumonidae actually do likely to be explained by chemical defence show anomalous diversity (Sääksjärvi et al., of their hosts, so-called nasty-host 2004; Quicke, 2012; Veijalainen et al., SONGVORAWIT ET AL. — TAXONOMIC PROGRESS AND DIVERSITY OF ICHNEUMONOID WASPS 85 TABLE 3. Comparison matrix of description rate of braconid wasps between countries in SEA by using k-sample Anderson-Darling test. Significant differences are indicated in bold (P < 0.05) and numbers in parentheses are the numbers of discovery event of new species or new country record until the end of 2019. BN ID LA MY MM PH SG TH VN (33) (604) (40) (482) (54) (412) (27) (377) (261) BN 10.95 2.07 8.25 5.02 22.74 1.92 25.97 7.81 ID 3.04 6.46 3.68 18.39 2.31 250.00 139.70 LA 1.93 0.97 8.96 0.41 36.33 15.97 MY 1.49 17.12 1.08 210.10 110.00 MM 5.44 0.47 46.68 20.88 PH 3.91 214.40 122.90 SG 28.08 11.94 TH 44.53 BN = Brunei, ID = Indonesia, LA = Laos, MY = Malaysia, MM = Myanmar, PH = the Philippines, SG = Singapore, TH = Thailand and VN = Vietnam 2012), and if they do, what the underlying curve of braconids in SEA continually reasons might be, and whether it is only a increases with acceleration after 2000 without feature of ichneumonid diversity. any sign of an asymptote. Previously, An alternative possibility is that the species richness of braconids in tropical observed low tropical diversity of Asia has been estimated there would be ichneumonids is due to bias in collecting approximately 2,500 species (Jones et al., and/or distribution of taxonomic effort 2009). So far, our results showed that the Furthermore, collection bias and description current number of described braconid bias is likely to reflect the wasp’s body size species is just a half of that prediction. In and this is also related to their biology as the case of Ichneumonidae, although the well as possibly differing between temperate estimation of species richness in SEA no and tropical zones (Quicke, 2012). As noted literature has not been reported, from the in the ‘Manual of the New World Genera of species accumulation curves in this study, the family Braconidae’ (Wharton et al., we believed that there are numerous 1997) many genera in North America are undescribed ichneumonids waiting to be thought to contain more undescribed than discovered. described species. On the other hand, most The shapes of the species accumulation areas in the tropics are still unexplored both curves reflect the impact of historical events due to the lack of experts and limited in a region. Early taxonomic research in accessibility to the areas (Quicke, 2012; many parts of the world are a legacy from Veijalainen et al., 2012). the colonial period (Patterson, 2001; Species accumulation curves are a way to Figueiredo and Smith, 2010). SEA was compare the progress of taxonomic studies directly affected by western colonialism between areas as well as providing a tool for from the 18th century to the middle of the predicting total species richness by fitting 20th century with France colonizing what are the curve to a model (Soberón and Llorente, now Cambodia, Laos and Vietnam, the 1993; Bebber et al., 2007). The accumulation British Empire dominating from India to 86 TROPICAL NATURAL HISTORY 21(1), APRIL 2021 TABLE 4. Comparison matrix of description rate of ichneumonid wasps between countries in SEA by using k- sample Anderson-Darling test. Significant differences are indicated in bold (P < 0.05) and numbers in parentheses are the numbers of discovery event of new species or new country record until the end of 2019. BN ID LA MY MM PH SG TH VN (42) (656) (114) (296) (162) (175) (55) (97) (345) BN 4.66 14.53 2.62 1.45 3.06 0.85 1.19 21.22 ID 107.00 3.85 3.10 2.92 3.51 19.07 231.40 LA 69.40 46.26 55.17 20.12 18.37 18.99 MY 1.81 1.57 2.14 11.12 133.20 MM 3.58 1.71 6.79 85.75 PH 1.47 9.82 109.80 SG 2.34 38.18 TH 25.71 BN = Brunei, ID = Indonesia, LA = Laos, MY = Malaysia, MM = Myanmar, PH = the Philippines, SG = Singapore, TH = Thailand and VN = Vietnam Myanmar and Malaysia and the Dutch in these areas might also be important much of Indonesia. During this period, contributing factors with geographic barriers naturalists and explorers from Europe, for limiting gene flow between islands, of both example, Alfred Russel Wallace (in parasitoids and their hosts, and so leading to Indonesia during 1854–1862), came to SEA high speciation rates (Witt and Maliakal‐Witt, for exploring resources, including plants and 2007; Santos et al., 2011). Furthermore, animals, and brought those specimens back Indonesia which has the highest species to museums in Europe causing a speed up of richness for both families, contains two new descriptions in this region during 1900– biogeographic realms, Sundaland and 1920 as shown in Fig. 2 (Wallace, 1869; Wallacea, which provides another possible Wolfe, 2006; Clement, 2016). However, the explanation of why its parasitoid diversity is description rate decreased from the 1930s to relatively high (Sodhi et al., 2004). the early of the 21st century. Part of this was Thailand and Vietnam are the countries due to the deaths and retirements of some that have contributed most to the increase of prolific European ichneumonoid taxonomists ichneumonoid records during the 21st who were most active, for example G. century. Thailand was never conquered by Szépligeti in Budapest and P. Cameron in western countries during colonial period London. World War II (1939–1945) also had a which had the consequence that the large impact and achieving independence of description of parasitoid wasps collected most countries in SEA resulting in stopping from this country remained very low until the taxonomic work of European naturalists recently, with little European involvement (Goto, 2003; Osborne, 2016). and no substantial local infrastructure such Indonesia, Malaysia and the Philippines as national museum collections on a scale have the highest number of ichneumonoid even remotely comparable to the major records, which is largely due to the colonial European institutions. Vietnam experienced legacy. However, geographical characteristics much unrest both from wars and invasion of such as the large number of archipelagos in foreign countries which had negative SONGVORAWIT ET AL. — TAXONOMIC PROGRESS AND DIVERSITY OF ICHNEUMONOID WASPS 87 FIGURE 3. Southeast Asian maps shaded to show the current number of braconid and ichneumonid wasp species per country. impacts on all aspects of biodiversity on taxonomic effort in countries such as research (Osborne, 2016). In these two Cambodia, Laos and Myanmar. Transportation countries, collaboration between western to rural areas and forests is limited and experts (such as DLJQ, Cornelis van requiring laborious work and an associated Achterberg and Michael J. Sharkey) and high level of expense. Some parts of the local taxonomists (such as Buntika Areekul region are still too dangerous to access due Butcher, Khuat Dang Long and Nhi Thi to the wartime legacies of land mines, and Pham) combined with increasing integration unexploded bombs together with other of molecular techniques for identification national security reasons such as drug (DNA barcoding), began after 1990. For trafficking (Chandler, 2008; Osborne, 2016). example, the description of 179 new Thai For example, the very low number of wasp braconid species from one genus (Aleiodes) species recorded from Cambodia is largely in a single publication by Butcher et al. due to the numerous unrest events following (2012), and the description of three new WWII, such as Cambodian Civil War genera and 42 new species of Vietnamese (1968–1975), Cambodian genocide by the braconids by Achterberg and Long (2010). Khmer Rouge regime (1975–1979) and These works alone represent large Cambodian–Vietnamese War (1978–1989). percentage increases in ichneumonoid Although current politics are more stable records within a short period of time. than in the past, it will likely be a long time Accessibility to the areas, the prevailing before some areas can be explored in depth political situation and impoverishment for entomology. probably had a marked negative influence 88 TROPICAL NATURAL HISTORY 21(1), APRIL 2021 FIGURE 4. Number of taxonomists involved in new species description or new records in SEA over periods of time. The taxonomic study of ichneumonoids involved ichneumonoid wasps (Meierotto et in SEA is increasing and, especially in al. 2019; Sharkey et al. 2021), and whilst Thailand and Vietnam, gaining more not without criticism, should be applied to attention than the past. The number of the SEA fauna to greatly expand the number taxonomists involved is considerably larger of species recorded from this region. now than before 1990. Moreover, there is now participation by local taxonomists ACKNOWLEDGEMENTS which never occurred before 1990. Although the proportion of the local taxonomists is This research was supported by the Rat- still much lower relative to the foreign chadapisek Somphot Fund for Postdoctoral experts, this is a good sign of taxonomic Fellowship, Chulalongkorn University to studies in parasitoid wasps in the region. NS and Sci-Super VI_63_001. Perhaps education and training local people to be taxonomists can improve information of parasitoid wasp diversity and emphasize LITERATURE CITED SEA as an important diversity hotspot in the world. However, it seems likely that Achterberg, C. van. and Long, K.D. 2010. Revision of the Agathidinae (Hymenoptera, Braconidae) of revolutionary approach to how species are Vietnam, with the description of forty-two new described will be needed, such as primary species and three new genera. ZooKeys, 54: 1-184. reliance on DNA barcode data and basic Anderson, T.W. and Darling, D.A. 1952. Asymptotic images (Meierotto et al. 2019). Significantly, theory of certain "goodness of fit" criteria based on stochastic processes. The Annals of the first applications of this procedure have Mathematical Statistics, 23: 193-212.