SCIENTIFIC CORRESPONDENCE

Bioacoustics or pitfall traps: comparison of a modern and traditional method to estimate richness

The order occurs in a variety urban residential area, site three (S3) had carried out previously. Cylindrical plas- of terrestrial ecosystems and serves as an scrubby vegetation characteristics of an tic pots of diameter 17 cm and depth important primary consumer and prey arid region with Prosopis sp. and Acacia 16 cm were used as pitfall to catch or- base for bats1, birds and spiders2. Or- sp. as dominant tree species and site four thopteran and other . Each pit was thopteran communities are affected by (S4) had regularly maintained landscaped covered with a funnel to make sure that vegetation structure and composition and gardens with seasonal flowering species the captured does not jump out. A respond strongly to changes in plant managed by civic authorities. The acous- non-invasive method of pitfall trap was community composition. Hence, they are tic and pitfall sampling were carried out used to avoid unnecessary killing of in- suitable for monitoring and conservation from January to April during 2013 and vertebrate species. Pitfall traps without studies3,4. A variety of sampling methods 2014 respectively. The temperatures any chemical preservative have been such as sweep netting, pitfall traps and ranged from 10C in January to 38C in demonstrated as a viable alternative to malaise traps or light traps are employed April, and relative humidity ranged from trap Orthoptera species previously17. for estimation of Orthoptera diversity 50% to 65% during the sampling months. Each trap was monitored every alternate and their abundance from a localized or Call of the ensiferan males was recor- day (spanning a period of 42 days) to over a large area5,6. Studies on transect ded in the field in the evening between check for captured insects. Captured count, quadrat sampling and sweep net- 6:00 and 9:00 pm. Individual calling in- invertebrates were photographed for tax- ting have been carried out mainly in sects were first tracked by ear and locat- onomic placement, and invertebrates grasshoppers and in a few cases in katy- ed. Recordings were made by holding a trapped in the pitfalls were counted and dids and field crickets for comparing digital recorder (TASCAM DR-08, released back in the field but away from efficiency of sampling methods in esti- TEAC, America Inc., USA, 44.1 kHz, 16 the pit. In case of Orthoptera, two indi- mating orthopteran diversity patterns7,8. bit, .wav format) at a distance of 25 cm viduals per species were preserved. A to- One of the most commonly employed from the calling . As the calling tal of 50 pits were laid for data techniques for collecting surface-active orthopterans are active only in the even- collection. However, over a period of invertebrates is pitfall trapping6. Howev- ing, the acoustic sampling was restricted time 27 pits were stolen and hence, sam- er, pitfall traps for Orthoptera species es- to 3 h per evening for a total of 42 days. pling had to be abandoned for these sites. timation have given mixed results due to Only two individuals of a call type were Hence a comparison between the two changes in vegetation structure8. Spe- preserved in 70% alcohol for taxonomic methodologies, i.e. acoustic and pitfall cies-specific calls of ensiferan insects identification and the rest were released sampling is limited to a period of four serve as a reliable method for species back in the place where they were cap- months. identification as each species has a tured. Song analysis was performed us- Orthopteran specimens were identified unique frequency and temporal pattern. ing the signal processing software up to the genus level using keys in Bioacoustics monitoring is widely used RAVEN Pro 1.4 (Cornell Lab of Orni- Chopard18. Other invertebrates were for Orthoptera species richness estima- thology, Ithaca, NY, USA) and Spectra classified till order level using entomol- tion9,10. Though studies on effectiveness Plus 5 (Pioneer Hill Software, Poulsbo, ogy keys19. A standardized abundance of of acoustic methods with respect to tradi- WA, USA) for temporal and spectral each taxon was estimated by dividing the tional methods have been carried out in analysis. number of individuals in each taxon by birds and amphibians, studies are lacking Pitfall traps were laid in the same loca- the sampling effort (number of pits) to in acoustically active insect groups11–13. tions where bioacoustics sampling was correct for unequal sampling effort in Also, distribution and abundance pattern of Orthoptera at an urban ecosystem lev- el has received little attention in India Table 1. Distribution of Ensifera species recorded using acoustic sampling 10,14–16 and worldwide . Ensifera species S1 S2 S3 S4 Total no. of individuals The aim of the present study is to (1) estimate species richness of Ensifera (In- 1. Superfamily: fraorder: Gryllidea) in Delhi and subur- Family: ban region using bioacoustics method; Gryllodes sp. 1 1 3 3 8 (2) Compare the bioacoustics method Gryllus bimaculatus – – – 1 1 and pitfall trapping in estimating species Gryllus X 1 1 2 2 6 richness of Ensifera (Infraorder: Gryllid- Gryllus Y – – – 1 1 Family: ea), and (3) quantify diversity of other Dianemobius sp. 1 1 3 1 6 invertebrates captured in the pitfall traps. The acoustic sampling of ensiferans 2. Superfamily: was carried out at four locations in Delhi Family: Gryllotalpidae region (28.6139N, 77.2090E). Site one Gryllotalpa sp. 1 1 1 2 5 (S1) was a predominantly undisturbed Total individuals 4 4 9 10 27 grassland area, site two (S2) was an

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SCIENTIFIC CORRESPONDENCE four sites owing to loss of pitfall traps. X (n = 6) and Y (n = 1). The spectrogram single family, i.e. Formicidae. Other The standardized abundances of various of calls of ensiferan species and their call orders of insects were Hemiptera with taxa were compared across four sites characteristics are provided in the Sup- 218 individuals, Blattodea with 420 indi- using a non-parametric test. plementary Material (Figure S1 and Ta- viduals, and Isoptera with 93 individuals A total of six ensiferan species were ble S1). Four ensiferan species (except (Figure 1). Only two Orthoptera species recorded using acoustic sampling. Five Gryllus sp. Y and Gryllus bimaculatus) with a total of 133 individuals were call types belonged to superfamily Gryl- were recorded from all sites (Table 1 and found from the 23 pitfalls. One genus be- loidea; four to family Gryllidae and supplementary Figure S2). longed to the family Gryllidae (Gryllodes one to Trigonidiidae, Dianemobius sp. A total of 7012 individuals of various sp.) in the suborder Ensifera and the oth- (n = 5). One call type belonged to super- invertebrate species were recorded from er belonged to suborder Caelifera. family Gryllotalpoidea (Gryllotalpa, 23 sampling pits. Individuals belonging All four sites were roughly equal in n = 5). Of the species belonging to fami- to two phyla, namely Arthropoda and abundance for various groups of inverte- ly Gryllidae, two species could be identi- Molluscs were captured from the pitfall brates in the pitfall traps (Kruskal wallis 2 fied up to the genus level, i.e. Gryllodes method. The most dominating order of  (3, N = 18) = 2.22, P = 0.53), except sp. (n = 8) and Gryllus bimaculatus insects was Coleoptera with 2302 indi- for class Chilipoda and order Isopoda in (n = 1). Two species belonging to the viduals, followed by order Hymenoptera class Insecta that were only found from same genus Gryllus have been referred as with 2250 individuals belonging to a S3 and grasshoppers in S1 (Table 2 and supplementary Figure S3). Interestingly, S3 with the highest diversity of inverte- brates in the pitfalls did not trap any en- siferan species, providing support to the disparity between the two sampling methods. Highest catch in pitfalls on S3 with higher sampling efforts but no or- thopteran species also indicates that the results are not a consequence of unequal sampling effort or loss of pitfalls in the area. In the present study only one species belonging to the family Gryllidae was observed from the pitfall sampling meth- od among a total of 7012 individuals, which is in contrast to the bioacoustics sampling carried out in the same region. This disparity between the two methods Figure 1. Pie chart showing (a) distribution of invertebrates found during pitfall sampling and could be ascribed to the sampling proce- (b) percentage of individuals captured in pitfalls belonging to orders in class Insecta. dure involved in each of them. The pit- falls were placed in a particular habitat frequented by ensiferan species and Table 2. Taxonomic classification and abundance of invertebrates captured in 23 pitfalls probability of collection depended on the across four sites in Delhi abundance of invertebrates in the region S1 S2 S3 S4 Total no. of and thus worked as a passive method of Invertebrates (3 pits) (3 pits) (11 pits) (6 pits) individuals capturing crickets. However, in the bioa- coustics method, a calling was 1. Phylum – Arthropoda actively searched and located through (i) Class – Insecta sound. This increases the chances of (a) Order – Orthoptera 63 20 0 0 133 finding even a single rare individual in (b) Order – Coleoptera 132 250 1370 550 2302 the habitat17. Also the acoustic sampling (c) Order – Hymenoptera 200 300 1000 750 2250 did not yield data on calling density or (d) Order – Hemiptera 58 20 60 80 218 abundance of calling species. Abundance (e) Order – Blattodea 0 60 310 50 420 (f) Order – Isoptera 0 63 0 30 93 of the six species recorded acoustically at (g) Order – Isopoda 0 0 1100 0 1100 the four sites could be estimated non- (ii) Class – Arachnida invasively using psychoacoustic sam- (a) Order – Araneae 0 3 5 305 313 pling by a trained listener, or by active (iii) Class – Chilipoda 0 0 28 0 28 playback from pitfall traps and by mark recapture methods. 2. Phylum – Mollusca Another reason for the difference in (i) Class – Gastropoda 0 0 125 30 155 the estimation of orthopteran species diversity in the two methods could be Total individuals 443 716 3998 1855 7012 due to microhabitat preference of ensi- Simpson’s index (1-D) 0.75 0.78 0.86 0.78 – ferans. Previous studies in India have

562 CURRENT SCIENCE, VOL. 113, NO. 4, 25 AUGUST 2017 SCIENTIFIC CORRESPONDENCE demonstrated that crickets and katydids 3. Batáry, P., Orci, K. M., Báldi, A., Kleijn, 18. Chopard, L., Fauna of India and the Ad- show preference for microhabitat10,20. D., Kisbenedek, T. and Erdős, S., Basic jacent Countries: Grylloidea, Baptist Ensifera species in this study were found Appl. Ecol., 2007, 8(3), 280–290. Mission Press, Calcutta, 1969. calling from cracks, crevices, and under 4. Stoner, K. J. and Joern, A., Ecol. Appl., 19. Brues, C. T. and Melander, A. L., Classi- the rocks and burrows in the ground. 2004, 14(5), 1306–1320. fication of Insects: A Key to the Known 5. Gardiner, T. and Hill, J., J. Orthoptera Families of Insects and other Terrestrial Such microhabitats were not covered Res., 2006, 15(1), 45–51. , Harvard University Press, during random pitfall sampling. A larger 6. Samways, M., McGeoch, M. A. and USA, 1932. number of randomly placed pitfall New, T. R., Insect Conservation: A 20. Jain, M. and Balakrishnan, R., Insect traps in varied microhabitats could pro- Handbook of Approaches and Methods, Conserv. Divers., 2011, 4(2), 152–155. bably remove this microhabitat-specific Oxford University Press, UK, 2009. bias. 7. Gardiner, T., Hill, J. and Chesmore, D., The present study also estimated J. Insect Conserv., 2005, 9(3), 151–173. ACKNOWLEDGEMENTS. S.D. and M.T. diversity of invertebrates other than 8. Schirmel, J., Buchholz, S. and Fartmann, thank the Science and Engineering Research Orthoptera collected in the pitfalls loca- T., J. Insect Conserv., 2010, 14(3), 289– Board, Department of Science and Technolo- ted in and around Delhi region. The 296. gy [SB/FT/LS-194/2012] and University of 9. Sueur, J. and Aubin, T., Syst. Entomol., Delhi [DRCH/R&D/2013-2014/4155] for res- overall invertebrate diversity was compa- 2003, 28(4), 481–492. earch funding. We thank the three anonymous rable across sites, except S3, which 10. Diwakar, S. and Balakrishnan, R., Bioa- reviewers for valuable suggestions that helped showed higher diversity due to the pres- coustics, 2007, 16(2), 113–135. improve the manuscript. ence of specific taxa. 11. Acevedo, M. A. and Villanueva-Rivera, L. The two sampling methods compared J., Wildl. Soc. Bull., 2006, 34(1), 211–214. and discussed here varied in the mode of 12. Celis‐Murillo, A., Deppe, J. L. and Received 26 July 2016; revised accepted 8 operation and each method provided Ward, M. P., J. Field Ornithol., 2012, June 2017 unique data on Orthoptera. The study 83(2), 166–179. 13. Klingbeil, B. T. and Willig, M. R., indicated use of multiple sampling tech- 1, PeerJ., 2015, 3, e973. MANISHA TOMAR * 2 niques for species inventory and moni- ABHAY PRATAP SINGH 5,6 14. Tandon, S. K. and Hazra, A. K., Faunal toring in a region . It can be further 1 Diversity in India (Order: Orthoptera), SWATI DIWAKAR strengthened with long-term sampling, ENVIS Center, Zoological Survey of larger sample sizes and sex segregation India, Kolkata, 1998, pp. 183–188. 1Department of Environmental Studies, for population level assessment. 15. McIntyre, N. E., Ann. Entomol. Soc. Am., University of Delhi, 2000, 93(4), 825–835. Delhi 110 007, India

16. Penone, C., Le Viol, I., Pellissier, V., Ju- 2Acharya Narendra Dev College, 1. Raghuram, H., Deb, R., Nandi, D. and lien, J. F., Bas, Y. and Kerbiriou, C., Govindpuri, Kalkaji, Balakrishnan, R., Proc. R. Soc. B, 2015, Conser. Biol., 2013, 27(5), 979–987. 282(1798), 20142319. 17. Divya, B. U., Metrani, S. and Balakrish- New Delhi 110 019, India 2. Belovsky, G. E. and Slade, J. B., Oikos, nan, R., J. Bombay Nat. Hist. Soc., 2005, *For correspondence. 1993, 68(2), 193–201. 102(1), 38–43. e-mail: [email protected]

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