Trabajo Científico Article

ISSN 0373-5680 (impresa), ISSN 1851-7471 (en línea) Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016

Breaking the rule: multiple patterns of scaling of sexual size dimorphism with body size in orthopteroid

BIDAU, Claudio J. 1, Alberto TAFFAREL2,3 & Elio R. CASTILLO2,3

1Paraná y Los Claveles, 3304 Garupá, Misiones, Argentina. E-mail: [email protected] 2,3Laboratorio de Genética Evolutiva. Instituto de Biología Subtropical (IBS) CONICET-Universi- dad Nacional de Misiones. Félix de Azara 1552, Piso 6°. CP3300. Posadas, Misiones Argentina. 2,3Comité Ejecutivo de Desarrollo e Innovación Tecnológica (CEDIT) Felix de Azara 1890, Piso 5º, Posadas, Misiones 3300, Argentina.

Quebrando la regla: multiples patrones alométricos de dimorfismo sexual de tama- ño en insectos ortopteroides

RESUMEN. El dimorfismo sexual de tamaño (SSD por sus siglas en inglés) es un fenómeno ampliamente distribuido en los animales y sin embargo, enigmático en cuanto a sus causas últimas y próximas y a las relaciones alométricas entre el SSD y el tamaño corporal (regla de Rensch). Analizamos el SSD a niveles intra- e interes- pecíficos en un número de especies y géneros representativos de los órdenes or- topteroides mayores: , , Mantodea, , Dermaptera, Isoptera, y Mantophasmatodea. La vasta mayoría de las especies mostraron SSD sesgado hacia las hembras, pero numerosas excepciones ocurren en cucarachas y dermápteros. La regla de Rensch y su inversa no constituyeron patrones comunes, tanto a nivel intraespecífico como interespecífico, con la mayoría de las especies y géneros mostrando una relación isométrica entre los tamaños de macho y hembra. En algunos casos, los patrones alométricos hallados podrían relacionarse con la va- riación geográfica del tamaño corporal. También demostramos que no todos los es- timadores de tamaño corporal producen el mismo grado de SSD y que el dimorfismo puede estar influenciado por un gran número de condiciones de vida y patrones de desarrollo ninfal. Finalmente, discutimos nuestros resultados en relación a modelos actuales de la evolución del dimorfismo sexual de tamaño en animales.

PALABRAS CLAVE. Tamaño corporal. Blattodea. Dermaptera. Mantodea. Man- tophasmatodea. Caracteres morfométricos. Orthoptera. Phasmatodea. Regla de Rensch. Alometría.

ABSTRACT. Sexual size dimorphism (SSD) although a widespread phenomenon among , is both enigmatic as to its proximate and ultimate causes and the scaling relationships between SSD and body size (Rensch’s rule). We analyzed SSD at the intra- and interspecific levels in a number of representative and genera of the major orthopteroid orders: Orthoptera, Phasmatodea, Mantodea, Blat- todea, Dermaptera, Isoptera, and Mantophasmatodea. The vast majority of the spe- cies showed female biased SSD but numerous exceptions occur in cockroaches and . Rensch’s rule and its converse are not common patterns at both, intra- and cross-species level, most species and genera showing an isometric relation- ship between male and female body sizes. In some but not all cases, the demon- strated allometric patterns could be related to geographic body size variation. We also showed that not all body size estimators produce the same degree of SSD and that dimorphism can be strongly influenced by a number of living conditions and the patterns of nymphal development. Finally, we discuss our results in relation to

Recibido: 14-I-2016; aceptado: 17-III-2016 11 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 current models of the evolution of sexual size dimorphism in animals.

KEY WORDS. Body size. Blattodea. Dermaptera. Mantodea. Mantophasmatodea. Morphometric traits. Orthoptera. Phasmatodea. Rensch’s rule. Scaling.

INTRODUCTION son, 1994; Fairbairn, 2013). SSD is a controversial aspect of evolutionary biology for several reasons. The length range of living systems is aston- On one side, although sexual selection has tradi- ishing: it spans 17 orders of magnitude from tionally been assumed as the key process behind DNA molecules to ecosystems; while organisms SSD, it is now well known that natural selection vary 7 orders of magnitude in length and 21 in can also produce size differences between males mass (Ellers, 2001). Insects have an impressive and females and that both processes are not com- body size range, from less than 0.2 mm in the pletely independent from one another (e.g. Isaac, parasitic wasp Dicopomorpha echmepterygis 2005; Carranza, 2009). This problem includes (Mymaridae) to ca. 360 mm in the stick- the study of the adaptive significance of SSD, the chani (). Body mass genetic constraints to its evolution, and its proxi- varies accordingly with females of the giant mate and ultimate causes (Fairbairn, 1997, 2007). weta, Deinacrida heteracantha (Anostostoma- Secondly, a problem which has not received a tidae) weighing more than 70 g (Björkman et satisfactory explanation is that of the allometric al., 2009). The enormous amount of scientific scaling of SSD with body size. Bernhard Rensch literature relative to body size reflects (1950, 1960) proposed that in phylogenetically re- the importance of this trait in biology. Almost lated species, SSD increases with general body every life history and ecological characteristic size when males are larger than females and of animals is correlated with body size (LaBar- decreases when females are larger. This pattern bera, 1986, 1989; Calder, 1996; Smith & Lyons, was termed Rensch´s rule by Abouheif & Fair- 2013) and in turn body size is strongly affected bairn (1997) but despite numerous studies in very by most ambient abiotic and biotic factors (Gas- diverse taxa (Fairbairn et al., 2007) there is little ton, 1991; Chown & Gaston, 2010, 2013; Price evidence to support this rule and no convincing et al., 2011). Thus, most physical, physiologi- mechanism for its operation has been proposed cal, ecological, and evolutionary processes are (Reiss, 1989; Webb & Freckleton, 2007; Bidau & highly dependent on size; these relationships Martí, 2008a; Martínez et al., 2014). are called scale effects or scaling. As defined Further problems regarding the scaling of by Barenblatt (2003), scaling “… describes a SSD with body size remain. In the first place, seemingly very simple situation: the existence there is the question of the taxonomic level at of a power-law relationship between certain which it is studied, and if Rensch’s rule operates variables y and x, y = Axα, where A, α are con- (if it does) in any taxonomic entity. Most studies stants.” This so-called allometric equation is of the scaling of SSD with body size either phylo- usually expressed in logarithmic form as log y = genetically-based or not have been performed log A + αlog x. The concept of allometric scal- across species at different levels (Fairbairn et ing was initially developed by Otto Snell (1892), al., 2007), and only a few intraspecifically as for D’Arcy Wentworth Thompson (1917), and Julian example, in insects, some and Huxley (1932) and resulted in numerous theo- beetles (e.g. Bidau & Martí, 2008b; Stillwell & retical and empirical investigations of the scal- Fox, 2009; Blanckenhorn et al., 2007a,b). An ing laws regulating the allometric relationship additional problem is that of the appropriate of many organismic traits with body size (e.g. measurements for analyzing SSD (Fairbairn, Schmidt-Nielsen, 1975, 1984; Brown & West, 2007). Is it the same using body mass or body 2005; Hoppeler & Weibel, 2005). length, or some other measurement (e.g. pro- Differences in body size between sexes (sexu- notum width, wing length) as a proxy for body al size dimorphism, SSD) are pervasive in the ani- size? Are SSDs for different measurements sig- mal kingdom and thus, a fundamental component nificantly correlated? (Martínez et al., 2014). of body size variation (e. g. Darwin, 1871; Anders- Orthopteroids do not only vary greatly in

12 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects size (Nasrecki, 2004; Bell et al., 2007; Whit- cliens (Stål) (6 populations, 56♂/58♀) (Table 1). man, 2008; Brock & Hasenpusch, 2009) but Most studies of geographic variation of body size also in the magnitude of SSD and in body of orthopteroids are based on different linear mea- shape (Hochkirch & Gröning, 2008; Bidau et surements. However, different authors use different al., 2013; Bidau, 2014). Furthermore, many estimators of body size. For example, body length species are fairly common, easy to collect, and and length of hind femur are commonly used mea- have large geographic distributions that allow surements but in some groups (e.g. and the sampling of several populations inhabiting Proscopiidae) researchers tend to favor measure- different or even contrasting environments (Bi- ments of the head and the pronotum as proxies for dau et al., 2012). The latter is relevant because body size. Body mass measurements are extreme- it has been suggested that in species showing ly rare in these insect groups thus, few cases of intraspecific geographic variation in body size body mass SSD were included in this study. Some (e.g. Bergmann’s rule [Bergmann, 1847]) there studies included only one measurement of body may exist a link between these patterns and the size while others, reported variation in male and scaling of SSD with body size (Blanckenhorn female size of up to 10-plus linear characters. The et al., 2006). In this sense orthopterans are an latter were especially favorable because allowed excellent model for the comparative analysis the comparison of degrees of SSD and Rensch’s of SSD and although a few studies have been rule in different traits. Data were obtained from performed (Bidau & Martí, 2008b), virtually published tables and, in a few cases, extrapolated nothing is known about patterns of SSD at the from graphs provided in the publication. The study intraspecific level regarding the points men- concentrates in species where data on a sufficient tioned in this Introduction. number of populations were available for statisti- The aim of this investigation is to analyze the cal analyses, although some cases included only magnitude of SSD, its scaling with body size, a few populations and this is indicated in the text. the comparison between different estimates of Whenever the information was available, geo- SSD, and the geographic variation of SSD in graphic data of each population (latitude, longitude several species of Orthoptera belonging to the and elevation) were recorded. The raw data in all suborders and , as well as analyses were male and female population means species of Mantodea, Phasmatodea, Blattodea, for each trait. These values were log-transformed Isoptera and Dermaptera, using new data as for the purpose of statistics. Mean body length val- well as published information. ues for each species as shown in Tables 1, 6, 8, and 9 were obtained from the published literature MATERIALS AND METHODS usually averaging data from several populations. In the case of those species reported here for the first 1. Data collection time, six linear measurements were obtained: body For the purposes of this paper we collected in- length, hind femur length, hind tibia length, length formation from the published scientific literature on of tegmina, pronotum length and pronotum height. geographic variation of body measurements of sev- b. Cross-species (interspecific analysis): In eral orthopteroid species from most of the orders to put each of the intraspecific analyses usually included in the orthopteroid assemblage within the context of the higher-order taxa to (Tables 1-9). We collected data for two purposes: which the species belong regarding body size a. Intraspecific analyses. The criteria used for and sexual size dimorphism, we collected data including species were that at least 5 geographi- on body length of a large number of species cally separated populations were studied, and that of Orthoptera, Phasmatodea, Mantodea, Blat- data on body size (either body length, body mass todea, and Dermaptera to produce cross-spe- or some adequate morphometric proxy) for both cies analyses of the scaling of SSD with body sexes were available for each population or sam- size, and graphs representing the variation of ple. Also, we included unpublished data on three SSD within each higher-order taxon (Tables 8, South American melanoplines (Orthoptera: Acridi- 9; Figs. 1, 2). A graph for the Orthoptera was dae: ), Dichroplus fuscus (Thunberg) not included because a comprehensive one has (17 populations, 193♂/133♀), Ronderosia bergii been recently published (Hochkirch & Gröning, (Stål) (19 populations, 152♂/108♀) and Scotussa 2008). Only data on male and female body

13 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 Table 1. Orthopteroid species for which scaling of sexual size dimorphism (SSD) was analyzed in this paper. In the column corresponding to Rensch’s rule, values in parentheses are the slopes of RMA re- gressions (see text). All measurements correspond to adult individuals. In the case of the two Isoptera species, measurements correspond to alates.

Higher order Species Location Body Body size SSD Rensch’s References taxa length trend trend rule (mm)

Acrididae, Dichroplus fuscus Argentina, M: 18.0 LON (+M.+F) LON (↓) Is (1.04) This paper Melanoplinae (Thunberg) Paraguay F: 20.1

Dichroplus pratensis Argentina M: 22.3 LAT (-M,-F) NP R (1.38) Bidau & Martí, Bruner F: 25.2 2007a, 2008b

Dichroplus pratensis Argentina M: 22.3 ELE (+M) ELE (↓) Is (1.04) Miño et al., hybrid zone F: 25.2 2011

Dichroplus vittatus Argentina M: 15.0 LAT (-M,-F) NP IR (0.77) Bidau & Martí, Bruner F: 21.5 2007b, 2008b

Melanoplus U.S.A. M: 19.0 ELE (-M. –F) ELE () IR Levy & Nufio, boulderensis Otte F: 23.0 2014

Melanoplus U.S.A. M: 20.8 ------IR (0.78) Orr, 1996 devastator Scudder/ F: 23.0 M. sanguinipes (Fabriicius)

Melanoplus U.S.A. M: 19.8 LAT (-M, -F) LAT (↑) Is (1.10) Parsons & femurrubrum (DeGeer) F: 26.0 Joern, 2014

Melanoplus U.S.A. M: 21.3 LAT (-M,-F) NP R (1.28) Orr, 1996; Roff sanguinipes (Fabricius) F: 24.2 ELE (-M, -F) & Mousseau, 2005

Neopedies brunneri Argentina M: 17.8 LON (-M, -F) NP Is (0.87) Romero et al., (Giglio-Tos) F: 21.4 ELE (-M, -F) 2014

Podisma sapporensis Japan M: 19.1 ?? ?? Is (0.89) Tatsuta & Shiraki F: 25.2 Akimoto, 1998

Ronderosia bergii (Stål) Argentina, M: 18.2 LON (-F) LAT (↑) Is (1.02) This paper Paraguay F: 23.4 ELE (-F)

Scotussa cliens (Stål) Argentina M: 24.3 LON (+F) LAT (↑) IR (0.58) This paper F: 31.2

Acrididae, Cornops aquaticum Argentina, M: 25.6 NP LON (↑) R (1.25) Adis et al., Leptysminae Bruner Brazil, F: 31.1 2008 Uruguay, Trinidad, South Africa

Acrididae, clavatus U.S.A. M: 17.3 ELE (-M. –F) ELE (↓) IR Levy & Nufio, (Thomas) F: 20.3 2014

Chorthippus cazurroi Spain M: 13.0 ELE (-M, -F) NP Is (0.98) Laiolo et al., (Bolivar) F: 18.0 2013

Chorthippus vagans Turkey M: 16.6 ?? NP Is (1.01) Ciplak et al., (Eversmann) F: 22.4 2008

Chorthippus yersini Spain M: 19.0 ELE (-F) ELE (↓) Is (0.92) Laiolo et al., Harz F: 25.0 2013

14 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects

Higher order Species Location Body Body size SSD Rensch’s References taxa length trend trend rule (mm)

Omocestus viridulus Switzerland M: 15.8 LAT (+M, +F) LON (↓) Is (0.81/0.98) Berner & (Linnaeus) F: 20.5 LON (-M, -F) ALR (↓) Blanckenhorn, ELE (-M, -F) 2006

Pseudochorthippus Spain, M: 15.0 NP* NP R (1.57) Laiolo et al., parallelus parallelus France F: 20.0 2013 (Zetterstedt)

Psudochorthippus France M: 13.0 ------R (1.36) Butlin & parallelus erythropus F: 17.5 Hewitt, 1985 (Faber)/ P.p. parallelus

Acrididae, Caledia captiva Australia M: 24.5 LAT (+F) LAT (↑) Is (1.06) Groeters & Acridinae (Fabricius) F: 30.0 Shaw, 1996

Acrididae, vittatum Australia M: 12.0 NP NP Is (0.94) Harris et al., Catantopinae (Sjösted) F: 16.0 2012

Acrididae, alutacea North M: 47.0 ------R (1.27) Hubbell, 1960 (Harris) America F: 59.0

Acrididae, miniata Turkey M: 19.5 ------NR Ciplak et al., Oedipodinae (Pallas) F: 24.3 2008

Xanthippus corallipes U.S.A. M: 43.0 ELE (-M, -F) ELE (↑) R (1.40) Ashby, 1997 (Haldeman) F: 62.0

Romaleidae, Romalea microptera U.S.A. M: 55.0 LON (-M, -F) NP Is (0.88) Huizenga et (Palisot de Beauvois) F: 65.0 LAT (-M,-F)* al., 2008

Pyrgomorphidae, variegatus Nigeria M: 34.8 LAT (+M) ELE (↑) Is (0.84) Bamidele & (Linnaeus) F: 38.3 Muse, 2012

Tettigoniidae, Metrioptera roeselii Sweden M: 20.0 LAT (+F) LAT (↑) Is (0.97) Holma, 2009 (Hagenbach) F: 22.0

Eobiana engelhardti Japan M: 26.0 LAT (-M, -F) LAT (↑) R (1.30) Higaki & (Uvarov) F: 29.0 Ando, 2002

Tettigoniidae, Poecilimon luschani Turkey M: 20.8 ELE (-M. –F) ELE (↑) IR? Ciplak et al., birandi Karabag F: 22.5 2008

Poecilimon thessalicus Greece M: 19.0 NP* LAT (↓) R (1.64) Lehmann Brunner von Wattenwyl F: 20.0 &Lehmann, 2008

Poecilimon veluchianus Greece M: 17.0 ELE (-M, -F) NP Is (1.09) Eweleit & veluchianus Ramme F: 19.0 Reinhold, 2014

Poecilimon veluchianus Greece M: 16.3 ELE (-F) ELE (↑) Is (0.90) Eweleit & minor Heller & Reinhold F: 17.1 Reinhold, 2014

Poecilimon veluchianus Greece --- NP NP Is (1.10) Eweleit & Ramme (both Reinhold, subspecies) 2014

Tettigoniidae, Conocephalus U.S.A: M: 12.1 LAT (-M. –F) NP Is (0.90) Wason & Conocephalinae spartinae (Fox) F: 13.0 Pennings, 2008

Orchelimum fidicinium U.S.A. M: 18.0 LAT (-M. –F) NP Is (0.88) Wason & Rehn & Hebard F: 16.5 Pennings, 2008

Gryllidae, Teleogryllus emma Japan M: 24.3 LAT (-M, -F) NP Is (1.04) Masaki, 1967 (Ohmachi & Matsuura) F: 21.4

15 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016

Higher order Species Location Body Body size SSD Rensch’s References taxa length trend trend rule (mm)

Velarifictorus micado Japan M: 15.3 LAT (-M, -F) NP R (1.25) Zeng & Zhu, (Saussure) F: 20.0 2014

Gryllidae, Polionemobius Japan M: 6.7 LAT (+M, +F) LAT (↑) IR (0.69) Masaki, 1978 Nemobiinae taprobanensis (Walker) F: 6.8

Gryllotalpidae, Neoscapteriscus U.S.A. M: 30.4 ------R (1.84)* Forrest, 1987 Scapteriscinae borellii Giglio-Tos F: 31.0

Anostostomatidae Hemiandrus pallitarsis New M: 22.0 LAT (-M,-F) LAT (↑) R (1.76) Chappell, (Walker) Zealand F: 23.0 2008

Blattodea- Eupolyphaga sinensis China M: 22.6 LAT(+M) LAT (↓) Is (0.96) Hu et al., 2011 Corydiidae (Walker) F: 29.0

Mantodea, Tenodera Japan M: 73.0 ------IR* Matsura et al., angustipennis F: 79.0 1975 (Saussure)

Isoptera, Reticulitermes speratus Japan M: 3.8 ------Is (0.88) Matsuura, Rhinotermitidae Kolbe F: 5.5 2006

Isoptera, Nasutitermes corniger Panama M: 6.8 ------Is (1.07) Thorne, 1983 Termitidae (Motschulsky) F: 6.9

M: male; F: female. LAT: latitude; LON: longitude; ELE: elevation. NP: no discernible pattern. -/+: indicate the sign of the cor- relation between male and female body size, and geographic coordinates and elevation. Arrows indicate if SSD increases or decreases with LAT, LON and ELE. R: Rensch’s rule; IR: converse Rensch’s rule; Is: Isometry. length of each species were considered, and equate for this type of analysis. The use of RMA only length measurements from tip of head to regression of log10 (male size) on log10 (female tip of abdomen were included. Measurements size) is also justified because RMA is symmetric were obtained from primary and secondary which means that a single regression line de- published sources on the basis of availability fines the bivariate relationship independently of and the meeting of our standard criterium for which variable is X and which is Y, and this is length measurement. the case for SSD comparisons: Rensch’s rule is 2. The analysis of sexual size dimorphism supported when the slope βRMA is significantly and testing of Rensch’s rule > 1.0, while slopes < 1.0 signal its reversion. Because SSD is practically always female- Slopes not significantly different from 1.0 indi- sex biased in the studied species as is the rule cate sexual isometry. We run the regressions in most orthopteroids, we used the simplest using the software of Bohonak & van der Linde SSD estimator which is the ratio of the arith- (2004). One-delete Jacknife estimates of a, β metic means of female size and male size that and r2 were obtained and 95% confidence in- produces SSD indices higher than 1.0. Three tervals were calculated by bootstrapping 10000 exceptions occurred within our sample: length times over cases. The RMA slope is significantly of pronotum and wing length SSD are male- different from 1.0 when the former value is not biased in the mole-cricket Scapteriscus borelli included within the calculated 95% confidence and the katydid Metrioptera roeselii (it could be intervals. In a few cases although the 1.0 values possible that, in the last case, sampling bias were included in the CI but so close to one of the is the cause of the observation), respectively, limits, the difference of the slope was consid- and head width in the cricket mi- ered significant. RMA regression was also em- cado (Table 2). The scaling of SSD with body ployed to investigate allometries between body size was analyzed using a Model II regression parts. Simultaneous autoregressions (SARs) method: Reduced Major Axis (RMA) regression; between body size and SSD variables (different ordinary least-squares (OLS) regression is inad- SSD indexes using various body size estima-

16 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects Table 2. Mean índices of sexual size dimorphism (SSD= female size/male size) of different traits for all taxa shown in Table 1. References as in Table 1 except *.

Species Trait (mean SSD) D. fuscus BL (1.27): F3L (1.28); T3L (1.30); TEL (1.22); PL (1.30); PH (1.30) D. pratensis BL (1.08); F3L (1.11); T3L (1.12); TEL (1.03); PL (1.11); PH (1.14) D. pratensis hybrid zone BL (1.04); F3L (1.06); T3L (1.10); TEL (0.99); PL (1.06); PH (1.08) D. vittatus BL (1.27); F3L (1.27); T3L (1.28); TEL (1.22); PL (1.41); PH (1.33) M. devastator /M. sanguinipes BL (1.03) M. femurrubrum F3L (1.14) M. sanguinipes F3L (1.06); TEL (1.03); PL (1.04) N. brunneri F3L (1.18); T3L (1.15); PL (1.15); TEL (1.11) P. sapporensis BL: (1.32); HL (1.41); HW (1.27); ED (2.08); F1L (1.16); F2L (1.23); F3L (1.52); T3L (1.59); PL (1.61); EL (1.22); TAT (0.85) R. bergii BL (1.23); F3L (1.25); T3L (1.28); TEL (1.16); PL (1.32); PH (1.33) S. cliens BL (1.22); F3L (1.23); T3L (1.23); TEL (1.14); PL (1.32); PH (1.28) C. aquaticum TL (1.20); BL (1.39); TEL (1.20) C. cazurroi BL (1.35) C. vagans BL (1.37); TEL (1.25); F3L (1.28) C. yersini BL (1.33) O. viridulus F3L (1.27/1.22); P. parallelus parallelus BL (1.37) P. parallelus erythropus/ P.p. parallelus F3L (1.06) C. captiva PL (1.33) P. vittatum F3L (1.27) S. alutacea PW (1.43) O. miniata BL (1.25); F3L (1.27); TEL (1.23) X. corallipes BM (3.33) R. microptera F3L (1.08); PL (1.15) Z. variegatus Bl (1.10) E. wagenknetchi* BL (1.53); F3L (1.34); F3W (1.31); TEL (1.28); TEW (1.51); HW (1.36); PL (1.52); PH (1.34); BM (3.13); DW (3.07) M. roeselii BL (1.20); F3L (1.09); T3L (1.12); F3W (1.04); TEL (0.67); HL (1.12); HW (1.15); PW (1.10); BM (1.47) E. engelhardti HW (1.08) P. luschani birandi BL (1.09) P. thessalicus F3L (1.09); T1L (1.05); PL (1.04) P. veluchianus veluchianus F3L (1.10) P. veluchianus minor F3L (1.12) P. veluchianus (both subspecies) F3L (1.11) C. spartinae T3L (1.09) O. fidicinium T3L (1.09) T. emma HW (1.00) V. micado HW (0.96); BW (1.11) P. taprobanensis HW (1.06) S. borellii PL (0.83)

17 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016

Species Trait (mean SSD) H. pallitarsis BL (1.06); F3L (1.04); HL (1.11); HW (1.12); FaL (1.14) E. sinensis BL (1.28); BW (1.72); PW (1.56) P. angustipenns BL (1.09) R. speratus DW (1.13) N. corniger DW (1.28)

BL: body length; TL: total length; BM: body mass; DW: dry weight; F1L: fore femur length; F2L: mid femur length; F3L: hind femur length; T3L: hind tibia length; TEL: tegmina length; TEW: tegmina width; PL: pronotum length; PH: prontum height; PW: prono- tum width; PH: pronotum height; HW: head width; HL: head length; ED: eye distance; EL: epiproct length; TAT: tenth abdominal tergum; FaL: fastigium length. *Elasmoderus wagenknetchi (Liebermann, 1942). Ref.: Cepeda-Pizarro et al., 2003. tors), and geographic coordinates and eleva- 6. Testing the effects of different rearing tion, were performed in SAM v.4.0 (Rangel et and ecological conditions on SSD al., 2010). follows Beccaloni (2015), Since it is well-known that body size is highly Brock (2015), Eades et al. (2015), Hopkins et affected by environmental conditions (e.g. Whit- al. (2015), and Otte et al. (2015). Final retrieval man, 2008) it is only reasonable to expect that dates are indicated. SSD will be similary affected. To test this hypoth- 3. A test of the differential variability hy- esis we obtained body size data of males and pothesis for Rensch’s rule females of several orthopteroid species that An expected condition for the operation of were laboratory-reared in different ambient con- Rensch’s rule is that males are more variable in ditions or that were studied in different ecologi- body size than females. If this condition holds, cal scenarios we expect that in those species showing the con- 7. Testing the effects of ontogenetic allom- verse Rensch’s rule, females should display the etry on final SSD highest variability while in those cases where the Assuming that differential rates of develop- relationship between male and female body size ment and number of nymphal stages affect the is isometric, both sexes should be equally vari- degree of adult SSD, we performed compari- able. In order to test this hypothesis, we calculat- sons of SSD during nymphal development of 10 ed male and female coefficients of variation (CV species of orthopteroid insects for which accu- = s/ *100 where s= standard deviation, and = rate measurements of different traits were per- arithmetic mean) of body size to produce a mea- formed at each nymphal instar and adult stage. sure⨰ of the differential inter-sex variability (∆CD).⨰ 4. SSD and Rensch’s rule in different traits RESULTS We tested Rensch’s rule for different linear morphometric characters using the above de- 1. Body size and sexual size dimorphism in scribed methodology in 7 species in order to the studied species test if differences of SSD for each character Because SSD could be influenced by body affected the scaling of with size (see below) we tried to cover the widest body size. Also, a large scale comparison was possible range of sizes among the study species performed in our Dermaptera sample to high- (Table 1). Within our sample, the smallest caelif- light a higher-order pattern of sexual dimor- erans were Phaulacridium vittatum (Sjöstedt) phism divergence comparing body length and (Catantopinae) and Myrmeleotettix maculates forceps length sexual dimorphism. (Thunberg) (Gomphocerinae), and the smallest 5. Intraspecific allometric scaling ensiferans, the tettigoniid Conocephalus spar- Because differences in static allometry within tinae (Fox) (Conocephalinae) and the cricket species are important factors in determining Polionemobius taprobanensis (Walker) (Nemo- SSD when different traits are used, we explored biinae) (Tables1, 4). The smallest species were these allometric patterns within four melano- the termites Reticulitermes speratus Kolbe and pline species using Ordinary Least Nasutitermes corniger (Motschulsky) (Table 1). Squares (OLS) regressions and paired-samples The largest species are represented by Roma- t-test comparisons. lea microptera (Palisot de Beauvois) (Roma-

18 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects leidae) and the acridids corallipes (Haldeman) (Oedipodinae) and Ornithacris tur- bida (Walker) (Cyrtacanthacridinae) within the Orthoptera, and the Japanese mantid Tenodera angustipennis Saussure (Tables 1, 6). It must be kept in mind that the mean lengths are averages of many individuals and populations; most spe- cies and especially those with large geographic distributions, show high variability in body length. SSD was calculated for all available measure- ments of each species. Most measurements are linear and in only a few cases, body mass or dry weight were available for male/female compari- son (Table 2). For the Orthoptera, female/male size ratios were in general higher in caeliferans than in ensiferans as it has been previously re- ported (see discussion). However, interspecies variation is high even between closely related species. For example, within the Dichro- plus, D. pratensis Bruner shows a body length SSD of 1.04-1.08 while its sister species D. vit- tatus Bruner and other congener, D. fuscus (Thunberg) are much more dimorphic (SSD= Fig. 1. Distribution of sexual size dimorphism for body size (female body length/male body length) in a. Phasmatodea. 1.27) (Table 2). Within the melanoplines stud- b. Mantodea. Arrows mark mean values. ied here, the most dimorphic species was Po- disma sapporensis Shiraki (Table 2). While the Melanoplinae show low to moderate SSD (see discussion) other caeliferans are characterized by higher levels of dimorphism as is the case of the Gomphocerinae represented in this work by several truxaline species all of them showing relatively high SSD values (Tables 1, 2, 6). In the few cases where body mass was available for calculating SSD, values were sig- nificantly higher than those for linear measure- ments (Tables 2, 6). For example, the oedipo- dine Xanthippus corallipes has a mean SSD index of 1.44 when body length is considered, but SSD= 3.33 for body mass (Table 2) reflect- ing the different dimensionality of the employed measurements. However, the difference beween both indexes are not always as high: in the katy- did Metrioptera roeselii (Hagenbach) BL SSD= 1.20 and BM SSD= 1.47, and in the cockroach Eupolyphaga sinensis (Walker) 1.28 and 1.76, respectively (Table 2). In one case, the cricket (Saussure), SSD for head width and body mass showed opposite direc- tions (Table 2 and see Discussion). Fig. 2. Distribution of sexual size dimorphism for body size (female body length/male body length) in a. Blattodea. b. In order to illustrate the wide variation in SSD Dermaptera. In b. White columns represent the distribution of in our study organisms, we contructed Figs. 1 sexual dimorphism for forceps length. Arrows mark mean values. and 2. The bar graphs clearly show the extent

19 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 and range of variation of SSD in the different enough, all three patterns were observed in polyneopteran orders discussed in this paper. three closely related species of a single genus, 2. Scaling of SSD with body size follows dif- Dichroplus Stål (Tables 1, 2). ferent patterns A further interesting observation pertains to Table 1 shows the results of RMA regressions the scaling of SSD with body size within hybrid between log10 (male size) and log10 (female zones. As a whole, D. pratensis follows Rensch’s size) for several orthopteran species, a cock- rule but the rule was not verified within a hybrid roach, a praying , and two termites. For zone between two chromosomal races which dif- each species, the regression slope (βRMA) and in body size and the degree of SSD (Table the 95% confidence intervals are shown. In all 1). Melanoplus sanguinipes (Fabricius) also fol- cases when it was possible, the slope for the lows Rensch’s rule but the analysis of a hybrid regression of male body length on female body zone between this species and M. devastator length is shown; in the rest of cases, the slope showed the converse pattern (Table 1). Finally, corresponds to the regression using the first Pseudochorthippus parallelus parallelus (Zetter- measurement shown in Table 2. Of the 45 ana- stedt) complies with Rensch’s rule and the same lyzed cases, Rensch’s rule (as indicated by a pattern was observed among populations of a slope significantly > 1.0) occurred in 12 (26.7%) hybrid zone with the subspecies Pseudochor- thus, SSD decreases as body size increases. In thippus parallelus erythropus (Faber) (Table 1). eight cases (17.8%) scaling of SSD with body 3. SSD scaling and morphometric variability size followed a converse trend (βRMA<1.0) in Because it has been considered that one of which dimorphism increases with body size. In the preconditions for Rensch’s rule is a higher the rest (55.5%), male and female body sizes variability of body size in males with respect to fe- scaled isometrically (βRMA =1.0). Interestingly males, we calculated the coefficients of variation

Table 3. Male and female coefficients of variation (CV= s/ *100) for morphometric traits used in the calculation of RMA regression slopes in species that follow Rensch’s rule, its converse, or show iso- metric scaling. M= male; F= female; ∆CV= male CV – female⨰ CV. References as in Table 1.

Rensch’s rule Converse Rensch’s rule Isometry Coefficient Coefficient Coefficient of variation of variation of variation Species M F ∆CV Species M F ∆CV Species M F ∆CV

D. pratensis 8.86 6.17 2.69 D. vittatus 6.84 9.04 -2.20 D. fuscus 4.27 3.40 0.87

M. sanguinipes 7.60 6.20 1.40 M. boulderensis 5.71 7.79 -2.08 R. bergii 6.91 6.57 0.34

C. aquaticum 5.69 4.60 1.09 M. devastator 7.78 5.79 1.99 C. cazurroi 5.66 6.56 -0.90

P. p. parallelus 8.46 5.30 3.16 S. cliens 3.13 4.42 -1.29 C. yersini 3.78 3.94 -0.16

P. p. erythropus 3.82 2.58 1.24 A. clavatus 9.82 9.05 0.77 C. captiva 3.78 3.47 0.31

S. alutacea 10.79 8.72 2.07 P. luschani 14.8 12.3 2.50 P. vittatum 3.87 4.35 -0,48

X. corallipes 5.41 3.77 1.64 P. taprobanensis 1.52 2.18 -0,66 R. microptera 8.97 10.07 -1.10

E. engelhardti 7.31 5.61 1.70 T. angustipennis 4.35 8.37 -4.02 Z. variegatus 3.30 3.84 -0,54

P. thessalicus 6.60 3.98 2.62 ------P. v. veluchianus 4.88 4.44 0.44

V. micado 6.32 4.44 1.88 ------P. v. minor 5.56 4.91 0.65

N. borellii 3.66 1.99 1.67 ------C. spartinae 9.62 10.1 -0,48

H. pallitarsis 7.14 4.67 2.47 ------O. fidicidium 6.92 7.88 -0,96

------T. emma 6.84 6.73 0.11

------E. sinensis 3.17 3.22 -0.05

------R. speratus 9.7 11.4 -1.70

------N. corniger 8.4 8.0 0.40

20 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects (CV) of the body size estimators of both sexes als and populations, a considerable variation (Table 3). In all cases where Rensch´s rule was in SSD indices occur in many of the species. verified, males were more variable than females. For example, although in some species differ- In the case of those taxa following the con- ent linear measurements produced practically verse to Rensch’s rule, females were more vari- identical SSD estimates (e. g. Melanoplus san- able than males in five species. Those cases in guinipes (Fabricius), Dichroplus pratensis), in which a higher CV was observed in males could others strikingly different indexes were obtained. be attributed to low sample size (Aeropedellus One clear case is that of Podisma sapporensis clavatus (Thomas) and Poecilimon luschani bi- where SSD ranges from a male biased 0.85 for randi Karabag) or to the fact that measurements the length of the tenth abdominal tergum, to were taken from populations within a hybrid 1.61 in the case of pronotum length while body zone (Melanoplus devastator Scudder). Those length produced 1.31 (Table 2). species where the scaling of SSD with body size Furthermore, variation in the scaling patterns was isometric did not show any consistent pat- of SSD with body size also occurs when different tern of body size variation in males and females. measurements are used in regression analyses. Furthermore, both sexes of these taxa showed Table 4 shows values of βRMA in seven melano- very similar levels of variability (Table 3). pline species for which several linear measure- 4. The use of different measurements may pro- ments were available in a variable number of duce different estimates of SSD and scaling patterns populations. It is evident that while some spe- The vast majority of measurements employed cies show a remarkable consistency regarding in this study are linear since these are the most the scaling pattern (e.g. D. fuscus, D. vittatus, frequently used by biologists when analyzing D. pratensis, R. bergii, and S. cliens) others do body size variation in orthopteroid insects. Body not (e.g. P. sapporensis and Neopedies brun- mass measurements are rare and for reasons neri (Giglio-Tos)) (Table 4). that will be discussed later, probably not the It is worth noting that despite the fact that dif- best for studying SSD (however see below). We ferent linear traits may show different degrees calculated SSD for all available measurements of sexual dimorphism, SSD tends to be highly in all taxa and the results are shown in Table 2. It correlated although exceptions do occur. How- can be seen that, considering that all SSD esti- ever, the distribution of SSD values of different mates were calculated using the same individu- traits are usually significantly different as dem-

Table 4. Scaling of sexual size dimorphism for several traits of seven species of melanopline grass- hoppers. References as in Table 1.

βRMA (95% Confidence Interval) SPECIES N BL F3L T3L TEL PL PH HL HW D. fuscus 17 1.04 (0.60- 0.89 0.98 0.81 1.04 1.15 ------1.45) (0.58-1.03) (0.56-1.32) (-1.06-1.35) (0.64-1.46) (0.52-1.79) D. pratensis 25 1.33 1.77 1.89 1.46 1.62 1.74 ------(0.98-1.68) (1.19-2.35) (1.17-2.60) (1.12-1.80) (1.13-2.11) (1.17-2.309 D. vittatus 19 0.77 0.75 0.70 0.71 (0.44- 0.88 0.66 (0.44------(0.55-0.99) (0.53-0.98) (0.48-0.92) 0.98) (0.59-1.16) 0.88) R. bergii 17 1.02 1.10 1.11 0.98 1.13 1.06 ------(0.68-1.66) (0.75-1.80) 0.77-1.74) (0.90-1.19) (0.77-1.77) (-0.95-1.78) P. sapporensis 14 --- 0.89 0.96 --- 0.63 --- 0.83 0.89 (0.79-1.09) (0.74-1.46) (0.33-0.94) (0.50-1.239 (0.63-0.98) S. cliens 6 0.58 0.57 0.66 0.60 0.58 0.77 ------(0.31-1.109 (0.30-0.99) (0.34-1.00) (0.35-1.44) (0.37-1.17) (0.09-1.23) N. brunneri 5 --- 0.86 0.39 0.97 0.57 ------(0.21-1.22) (0.29-1.56) (0.66-1.29) (-0.35-0.81)

N: number of populations; BL: body length; F3L: hind femur length: T3L: hind tibia length; TEL: tegmina length; PL: pronotum length; PH: pronotum height; HL: head length; HW: head width.

21 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 Table 5. A. Allometric scaling of 5 morphometric traits with body length in four species of melano- pline grasshoppers. B. Correlations between SSD for body length and SSD for six linear traits, and the respective paired t-tests in the same species.

Trait A. F3L T3L TeL PL PH Species nM/F bM bF t ; p bM bF t ; p bM bF t ; p bM bF t ; p bM bF t ; p Dichroplus 193/121 0.890 0.868 5.41; 0.695 0.772 6.21; 0.766 0.807 2.34; 0.786 0.974 31.4; 0.757 0.624 2.96; fuscus <0.001 <0.001 <0.05 <0.001 <0.005 Ronderosia 155/93 0.687 0.948 27.99; 0.694 0.948 33.81; 0.865 1.277 17.72; 0.744 0.835 40.53; 0.696 0.838 25.02; bergii <0.001 <0.001 <0.001 <0.001 <0.001 Scotussa 95/53 0.835 0.901 1-44; ns 0.844 0.866 0.94; 0.724 0.662 11.77; 0.927 0.906 3.74; 0.906 0.860 3.84; cliens ns >0.001 <0.001 <0.001 Dichromatos 40/57 0.871 0.739 3.38; 0.809 0.823 0.23; ns 1-358 1.226 2-56; 0.859 0.860 ≅0; 1-190 0.617 13.51; lilloanus =0.001 <0.05 ns <0.001 SSD BL/F3L SSD BL/T3L SSD BL/TeL SSD BL/PL SSD BL/PH B. R2 Pair. t p R2 Pair.t p R2 Pair.t p R2 Pair. t p R2 Pair. t p Dichroplus 0.68** 3.29 <0.05 0.49* 5.44 <0.001 0.14ns 2.67 <0.05 0.20ns 3.53 <0.05 0.70** 3.62 <0.05 fuscus Ronderosia 0.84** 1.97 ns 0.87** 5.43 <0.001 0.37* 4.94 <0.001 0.79** 6.12 <0.001 0.59** 4.65 <0.001 bergii Scotussa 0.74* 1.40 ns 0.84* 1.52 ns 0.52ns 4.82 <0.001 0.67* 5.50 <0.001 0.41ns 3.11 <0.05 cliens Dichromatos 0.41ns 1.25 ns 0.44ns 3.31 <0.05 0.13ns 1.66 ns 0.69* 3.99 <0.005 0.19ns 2.42 <0.05 lilloanus

F3L: femur 3 length; T3L: tibia 3 length; TeL: tegmina length; PL: pronotum length; PH: pronotum height; nM/F: number of males and females measured; bM, bF: slopes of OLS regressions between log10 (trait) and log10 (body length); t,p: Student´s t-statistic for the difference between male and female slopes and its significance; R2: coefficient of determination; Pair.t: t-statistic for the paired t-tests between SSDs; p: statistical significance. onstrated by paired t-test comparison (Table 5). maptera show a large number of species with If the growth of different body organs were iso- little or no SSD with respect to body length and metric in both sexes we would not expect differ- almost equivalent numbers of species with ences in SSD for different linear traits. However, male-biased and female-biased SSD (see Dis- most structures show allometric growth and, if cussion and Fig. 2b). However, earwigs have differential sexual allometry occurs, then unequal conspicuous forceps-like cerci which can be SSD estimates could be obtained for different extremely dimorphic in size and form. As shown body parts. To analyze this problem we studied in Fig. 2b sexual dimorphism of forceps length static allometry in relation to SSD of six linear mor- follows a completely different distribution from phometric characters in 4 grasshopper species that of SSD for body length. Furthermore, aver- using individual (not population averages) mea- age body length SSD is, in our sample, 1.04, surements. Results are shown in Table 5. It can be and sexual dimorphism for forceps length, 0.85. seen that for most traits, males and females have Both SSDs are not significantly correlated (R2= different patterns of allometric growth (as shown 0.005; p= 0.235). A second selected example by significant differences between the slopes of of this situation is that of the bark mantid genus OLS regressions of log10 [trait] on log10 [body Liturgusa Saussure, which as all Mantodea pos- length]) and the degree of variation in SSD esti- sesses highly specialized hunting forelegs (see mates is associated with these differences. Table 9). Mean SSD (range) for six morphomet- A more dramatic case of the disparity be- ric characters (data from Svenson, 2014) were: tween sexual dimorphism for body size and body length, 1.29 (1.14-1.63); prothoracic femur specific body parts is found in earwigs. Differ- (F1) length, 1.26 (1.12-1.55); mesothoracic fe- ently from other orthopteroid orders, the Der- mur (F2) length, 1.15 (1.04-1.27); metathoracic

22 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects Table 6. Effects on sexual size dimorphism (SSD= female size/male size) of different living and rear- ing conditions in twelve species of orthopteroid insects.

SPECIES LOCATION BODY SIZE CONDITION F3L TEL PL HW BM References (mm) Schistocerca Barbados M.: 42 ISOLATED 1.25 1.23 1.27 1.19 1.92 Antoniou & pallens (Thunberg) F: 52 Robinson, 1974 CROWDED 1.20 1.20 1.22 1.20 1.67 Ornithacris turbida Africa M.: 50 ISOLATED 1.19 1.19 --- 1.15 1.69 Antoniou, 1973 (Walker) F: 61 CROWDED 1.23 1.23 1.18 1.89 Melanoplus U.S.A. M.: 31.5 ISOLATED 1.27 1.17 1.29 1.25 --- Dingle & Haskell, differentialis F: 36.5 1967 (Thomas) CROWDED 1.20 1.14 1.14 1.17 Acheta domesticus Canada M.: 25.0 ISOLATED ------1.06 McFarlane, 1962 (Linnaeus) F: 30.0 CROWDED ------1.06 Locusta migratoria Africa, Asia M.: 37.5 ALBINO ISOLATED 1.19 1.22 1.19 1.22 -- Hoste et al., (Linnaeus) F: 50.0 2002 ALBINO CROWDED 1.11 1.14 1.14 1.15 --- NORMAL ISOLATED 1.16 1.23 1.16 1.23 --- NORMAL 1.06 1.08 1.09 1.11 --- CROWDED Anabrus simplex U.S.A. M: 41.0 HIGH DENSITY ------1.013 --- 1.48 Gwynne, 1984 Haldeman Greystone F: 45.0 U.S.A., Indian LOW DENSITY ------1.008 --- 1.26 Meadows Schistocerca U.S.A., Portal M: 41.5 Prosopis ------1.41 Sword & shoshone (Thomas) F: 58.0 Simmondsia 1.49 Chapman, 1994 U.S.A., Tacna Prosopis ------1.67 Simmondsia 1.49 Chorthippus England M.:15.5 25°C 1.16 ------1.45 Willott & Hassall, brunneus F: 20.0 30°C 1.22 1.67 1998 (Thunberg) 35°C 1.28 1.92 England M.:15.8 25°C 1-11 ------1.27 Willott & Hassall, viridulus (Linnaeus) F: 20.5 30°C 1.25 1.67 1998 35°C 1.25 1.72 Myrmeleotettix England M.:11.5 30°C 1.15 ------1.35 Willott & Hassall, maculatus F: 13.5 35°C 1.16 1.43 1998 (Thunberg) Stenobothrus England M: 16.5 30°C 1.10 ------1.41 Willott & Hassall, lineatus (Panzer) F: 23.0 35°C 1.15 1.54 1998 Blatella germanica Germany M.:13.5 24°C 1.02 1.10 ------1.30 Reinhard, 2007 (Linnaeus) F: 20.0 27°C 1.06 1.12 1.25 33°C 1.09 1.12 1.28 Chorthippus Belgium M.:15.5 URBAN 1.20 1.18 ------2.44 San Martin y brunneus F: 20.0 RURAL 1.19 1.16 2.44 Gomez & Van (Thunberg) Dyck, 2002 Pholidoptera Slovakia M.:15.5 ISO1 1.08 --- 1.07 --- 1.25 Fabriciusová et fryvaldszkyi F: 20.0 ISO2 0.99 0.97 1.00 al., 2008 (Herman) ISO3 1.11 1.08 1.43 Oedaleus Africa M.:29-0 G1 1.24 1.30 1.25 1.32 --- Ritchie, 1981 senegalensis F: 38.6 G2 1.26 1.31 1.27 1.33 (Krauss)

M: male; F: female; F3L: hind femur length; TEL: tegmina length; PL: pronotum length; HW: head width; BM: body mass. G: generation; ISO: isolated population.

23 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 femur (F3) length, 1.14 (1.02-1.29); and prono- adult size of males and females and changes tum (P) length, 1.24 (1.15-1.44). The converse in the degree of SSD. However, these changes Rensch’s rule was verified for body length seem to be species specific as shown by the (βRMA= 0.70 [0.51-0.94]), and F1 (βRMA= effects of rearing in isolation or crowded condi- 0.59 [0.49-0.81]) while the other three charac- tions in four orthopteran species. While SSD de- ters showed sexual isometry; F2 (βRMA= 0.85 creases in crowded conditions in Schistocerca [0.69-1.01]), F3 (βRMA= 0.999 [0.76-1.14]), and pallens (Thunberg) and two strains of Locusta P (βRMA= 0.91 [0.74-1.08]) migratoria (Linnaeus), it has the opposite ef- 5. Geographic variation of SSD within species fect in Ornithacris turbida while no differences Many of the species studied by us showed in SSD were observed in a study of Acheta do- significant clinal variation in body size along mesticus (Linnaeus). Regarding diet, opposite latitudinal, elevational and/or longitudinal geo- effects were obtained when locusts, Schisto- graphic gradients (Table 1). The most frequent cerca shoshone (Thomas) from two different trends involved a decrease in size towards high- populations were made to feed on two different er latitudes or elevations although other patterns plant species (Table 6). Increasing rearing tem- or the lack of a pattern, were observed (Table perature produced parallel effects in four spe- 1). Because SSD could be affected by these cies of gomphocerine grasshoppers, that is, an body size clines, we analyzed if significant SSD increase of SSD while no significant differences geographic clines also existed. As shown in were observed in the cockroach Blatella ger- Table 1, in at least 19 cases, SSD clines along manica (Linnaeus) (Table 6). the geographic coordinates and elevation were 8. SSD and nymphal development observed usually in coincidence with body size Final adult size of insects, and thus SSD, is clines although the existence of the latter did not determined during development. As hemime- always imply SSD clines. tabolus insects, orthopteroids reach adulthood 6. Temporal Variation of SSD after a number of nymphal stages which var- The vast majority of species analyzed by us ies among species. We studied SSD for sev- are univoltine. However, there is an exception eral characters during nymphal development of represented by the mole cricket Neoscapter- seven orthopteran species (Table 7). The num- iscus borellii (Giglio-Tos) which has more than ber of nymphal stages varied widely (4-11) in one generation per year. It is most interesting the studied species. What all analyzed cases that this species follows Rensch’s rule not spa- have in common is that during a large part of tially (data used in this study come from the development nymphs show no SSD or reversed same population at different times of the year) SSD and that final female-biased dimorphism is but temporally since different generations show reached during the final developmental stages. different body sizes and SSDs (Table 1). Many In some species, this occurs mainly because fe- bi- or multivoltine grasshoppers also show dif- males add a further instar (e.g. Bryophyma deb- ferences in size and SSD between genera- lis (Karsch), Chorthippus brunneus (Thunberg), tions as is the case of Oedaleus senegalensis plorans meridionalis Uvarov, (Krauss) in which two consecutive adult gen- and Atractomorpha sinensis sinensis Bolívar) erations showed a 12% increase in body size of not present in males, while in other species both sexes and a slight but significant increase where males and females share the same num- of SSD in all studied characters (Table 6). ber of nymphal stages (e.g. lepro- 7. Different ecological and/or rearing con- sus (Fabricius), Deinacrida White spp.), there is ditions can change SSD a fixed moment when female-biased SSD starts Different living conditions such as different to incresase until reaching the adult value (Table diets or rearing temperatures can modify adult 7). The situation is further complicated in cases body size of insects, thus potentially altering such as the mantid Psudomantis albofimbriata SSD. We analyzed different situations in which Stål where although males experience one extra orthopteroid populations experienced divergent nymphal stage adults nevertheless reach high living conditions (Table 6). In almost all studied female-biased SSD (Table 7). In another pray- cases, changes in diet, rearing temperature or ing mantis the developmental outcome is even environment produced modifications of final more complicated because nymphs of both

24 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects Table 7. Sexual size dimorphism (SSD) of different traits in seven orthopteran species. SSD calcu- lated as female size/male size is shown for each instar. Final (adult) SSD is indicated in bold type.

Instar number

Species N of Trait 1 2 3 4 5 6 7 8 9 10 11 Ref. Instars

Phymateus leprosus M: 10 BL 0.95 0.90 0.90 1.03 1.00 0.93 1.11 1.18 1.23 1.20 1 (Fabricius) F: 10

F3L 1.02 1.05 0.97 1.06 1.05 1.01 1.05 0.99 1.06 1.05

Bryophyma debilis M: 5 BL 0.96 0.99 1.04 0.97 0.99 1.45 2 (Karsch) F: 6

BM 1.00 0.94 1.09 1.11 0.93 1.19

PL 0.89 1.03 1.00 0.89 1.01 1.30

F3L 0.92 1.04 1.03 0.96 0.94 1.30

Chorthippus M: 4 F3l 1.01 1.05 1.23 1.28 3 brunneus F: 4, 5 (Thunberg)

BM 0.87 0.76 1.46 1.72

Eyprepocnemis M: 7 HW1 1.07 1.05 1.05 1.1 1.14 1.16 1.19 4 plorans meridionalis F: 7, 8 Uvarov

HW2 1.04 0.97 1.02 1.02 1.01 1.05 1.13 1.31

Atractomorpha M: 6 A 0.97 1.03 1.02 0.81 0.81 0.88 0.99 5 sinensis sinensis F: 7 Bolívar

PL 0.91 1.03 0.98 0.88 0.98 1.22 1.30

HWP 1.00 0.93 1.08 0.38 0.56 1.05 1.16

F3L 1.04 1.06 1.01 0.88 0.95 1.06 1.22

Deinacrida fallai M: 10 F3L 1.00 1.00 1.00 1.00 1.00 1.19 1.15 1.36 1.23 1.26 6 Salmon F: 10

BM 1.00 1.00 1.00 1.00 1.08 1.07 1.06 2.00 2.50 2.22

Deinacrida M: 11 F3L 1.00 1.00 1.00 1.13 0.88 0.84 0.97 0.98 1.04 1.17 1.14 6 heteracantha White F: 11

BM 1.00 1.00 1.00 1.00 1.14 1.20 1.00 1.00 1.17 1.73 1.73

Pseudomantis M: 7 PL 1.05 1.40 1.45 1.49 1.42 1.38 1.20 7 albofimbriata Stål F: 6

Hierodula majuscula M: 9 PL 1.00 1.00 1.00 1.00 1.00 0.95 0.96 0.97 1.08 1.39 7 Tindale F: 10

Stagmomantis M: 6,7 PL ------0.98 1.36 1.43 8 limbata Hahn F: 7,8

PL ------1.10 1.18 1.28

PL ------0.88 1.21 1.57 1.62

PL ------0.99 1.05 1.36 1.47

Higher order taxonomy of species: P. leprosus (Pyromorphidae: Pyrgomorphinae); B. debilis (Acrididae: Cyrtacanthacridinae);C. brunneus (Acrididae: Gomphocerinae); E. plorans (Acrididae: Eyprepocnemidinae); A. sinensis (Pyromorphidae: Pyrgomorphi- nae); D. fallai, D. heteracantha (Anostostomatidae: Deinacridinae); P. albofimbriata, H. majuscule, S. limbata (Mantidae, Man- tinae): References: 1. Kohler et al., 2008; 2. Luong-Skovmand & Balança, 1999; 3. Hassall & Grayson, 1987; 4. Jago, 1963; 5. Kevan & Lee, 1974; 6. Richards, 1973; 7. Allen et al., 2013; 8. Maxwell, 2014. Abbreviations: BL, body length; BM, body mass; F3L, hind femur length; HW, head width; A, antenna; PL, pronotum length; HWP, hind wing pad.

25 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 sexes may experience a variable number of in- sic natural selection. Sexual selection operates stars in the same population; thus, the degree of via two processes: intrasexual selection where SSD depends on what categories of males and individuals of one sex compete in various ways females are compared (Table 7). for the access to individuals of the opposite sex, and intersexual or epigamic selection that DISCUSSION involves choice of the members of one sex by members of the other sex (Darwin, 1871; Ander- Sexual dimorphism is arguably the most per- sson, 1994; Kokko et al., 2006; Clutton-Brock, vasive characteristic of bisexual organisms and 2009). A further proposed cause for SSD espe- was the main inspiration of Darwin’s (1871) the- cially apt for female-biased SSD is fecundity se- ory of sexual selection. Sexual dimorphism has lection (Honek, 1993; Reeve & Fairbairn, 1999) multiple manifestations as differences between although a positive relationship between body males and females in secondary sexual charac- size and fertility has also been documented for ters. Although the latter have been difficult to de- male insects (e.g. bush crickets; Wedell, 1997). fine precisely (e.g. Darwin, 1871; Cunningham, Natural selection could be the cause of SSD 1900; Morgan, 1919) a simple definition would in cases of niche partitioning between males be “Differences between males and females of and females (sexual segregation) (Shine, 1989; a species in size, structure, color, ornament, or Isaac, 2005). However, the effects of sexual and other morphological trait(s), not including the natural selection are frequently very difficult to sex organs” (Broughman, 2014), although di- discriminate, hence, some authors have pro- morphism is also manifested in behavioral or posed to eliminate the distinction between both biochemical traits. One of the most conspicu- forms of selection and concentrate on “con- ous types of sex dimorphism is constituted by trasts in the components, intensity and targets differences in size between males and females. of selection between males and females’’ (Clut- Sexual size dimorphism (SSD) can be slight and ton-Brock, 2010). In this sense, the “differential barely perceptible, or spectacular with members equilibrium hypothesis” of SSD proposes that of one sex many times larger or heavier than the males and females are differential targets of op- other (Fairbairn, 2013). Additionally, both sexes posing selective forces that shape SSD (Blanck- frequently differ in the size of specific body parts enhorn, 2005; Hochkirch & Grõning, 2008). A (sexual body component dimorphism or SBCD) further complication is represented by the mul- which are sometimes used to estimate the de- tiple proximate mechanisms that can determine gree of SSD (Fox et al., 2015): SSD may be male- differences in size between the sexes: in insects biased or female-biased which is the case of for instance protandry may favor smaller males the majority of invertebrates including insects (e.g. Morbey & Ydenberg, 2001; Bidau & Martí, (although exceptions do occur; see below) (e.g. 2007a, b; Blanckenhorn et al., 2007a, b) while Andersson, 1994; Faibairn et al., 2007; Fairbairn, a greater number of larval or nymphal stages 2013), while SBCD may not always follow the and longer development may produce larger same direction as SSD (Fox et al., 2015). females (e.g. Teder & Tammaru, 2005; Esperk Despite the enormous quantity of studies of et al., 2007; Tammaru et al., 2010; Teder, 2014). SSD in all kinds of species since Darwin´s time, The other problem that has generated a prof- the phenomenon remains largely an enigma fuse literature is that of the scaling of SSD with (Fairbairn, 2007, 2013). The studies of SSD body size essentially derived from Rensch’s roughly involve two main problems (Reiss, 1986, hypothesis (Rensch, 1950, 1960) later termed 1989; Andersson, 1994; Fairbairn et al., 2007). Rensch’s rule (Abouheif & Fairbairn, 1997). One is that of the ultimate causes of SSD where However, as Reiss (1986, 1989) has pointed both sexual selection and natural selection have out, Rensch’s original data are not statistically been variously favored since Darwin’s time. significant. Furthermore, many studies have While Darwin (1871) proposed sexual selection failed to prove an allometric scaling of SSD with as the main (but not unique) mechanism behind body size in the sense of Rensch’s rule espe- SSD and other forms of sexual dimorphism, cially when females are larger than males (e.g. Wallace (1889) considered that the vast majority Webb & Freckleton, 2007; Bidau et al., 2013) of cases could be explained essentially by clas- but also when SSD is male-biased (Lindenfors

26 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects Table 8. Scaling of sexual size dimorphism with body size in assorted families and of orthopteran insects. In columns 5, 6 and 7 mean male and female body lengths (BL) and average SSD are given. Values in parentheses represent the respective ranges. In the last column, the slope (β) of the RMA regression of log10 (male BL) on log10 (femaleBL) and the 95% confidence intervals (in parentheses) are shown. In bold type, taxa that follow Rensch’s rule or its converse. The extensive bib- liography consulted for the construction of this Table is readily available from the corresponding author.

ORDER N° OF MALE BL FEMALE BL BL SSD βRMA TAXA [F/M] Orthoptera Tristiridae 22 18.8 23.8 1.29 1.105 (Caelifera) (6.9-34.9) (10.0-39.6) (1.00-1.69) (0.93-1.28) Ommexechidae 24 15.9 22.6 1.46 1.075 (5.2-25.8) (8.6-36.6) (1.19-2.73) (0.95-1.24) Proscopiidae* 60 ------1.33 0.967 (0.79-1.70) (0.90-1.05) Tetrigidae 89 8.2 10.2 1.25 1.053 (5.3-13.3) (7.0-14.7) (0.97-1.57) (0.92-1.19) 195 30.1 42.9 1.43 0.953 (11.9-87.5) (14.1-109.3) (1.03-1.95) (0.91-0.99) Pamphagidae 43 28.9 43.4 1.52 1.024 (16.5-55.0) (25.5-77.0) (1.12-2.20) (0.87-1.20) Acrididae Catantopinae 140 17.9 23.7 1.33 0.980 (10.2-46.9) (13.1-59.0) (1.07-2.00) (0.92-1.04) Oedipodinae 221 21.1 28.1 1.35 1.092 (13.0-42.0) (17.8-53.0) (0.96-2.52) (1.01-1.18) Gomphocerinae 206 15.7 21.1 1.35 0.965 (8.2-28.0) (12.5-36.0) (1.00-2.12) (0.90-1.05) Melanoplinae 798 18.8 23.8 1.27 0.968 (9.0-34.5) (12.8-44.0) (1.01-1.83) (0.94-1.01) Orthoptera Tettigoniidae Phaneropterinae 115 19.2 20.9 1.10 1.042 (Ensifera) (7.3-37.0) (7.8-36.5) (0.90-1.63) (0.96-1.11) Decticinae 163 20.5 22.5 1.10 1.001 (9.3-47.5) (9.8-50.3) (0.92-1.43) (0.96-1.04) Ephippigerinae 62 26.4 28.0 1.06 1.023 (15.3-43.5) (16.2-41) (0.85-1.22) (0.92-1.14) Rhaphidiophoridae 27 17.9 18.3 1.03 1.085 (12.5-34.0) (12.5-31.5) (0.76-1.24) (0.85-1.26) Gryllidae 65 11.5 12.1 1.07 1.041 (2.2-34.5) (2.2-36.5) (0.86-1.39) (1.01-1.09) *SSD was calculated using pronotum length and not total body length. et al., 2007; Martínez et al., 2014; Martínez & body length (e.g. Prete et al., 1999; Bell et al., Bidau, 2016). This is particularly true for insects 2007; Whitman, 2008; Brock & Hasenpusch, (Blanckenhorn et al., 2007b). Thus far, no con- 2009; Bignell et al., 2011). Also, the vast major- vincing explanatory mechanism for Rensch’s ity of species in all orthopteroid orders shows rule (at least in the cases in which it seems to SSD. As in most insects, SSD is frequently fe- operate) has been postulated (Reiss, 1986, male-biased but cases of male-biased SSD also 1989; Martínez et al., 2014). occur in some orders (e.g. Blanckenhorn et al., The large assemblage of Neopteran insects 2007a, b; Hochkirch & Gröning, 2008; Chown referred to as “orthopteroids” shows a striking & Gaston, 2010). The distribution of SSD within amplitude of body sizes from tiny (less than 5 orthopteroid orders has seldom been analyzed mm long) ant-inquiline crickets and termites to (Sivinski, 1978; Hochkirch & Gröning, 2008; Bi- giant stick insects exceeding 300 mm in total dau et al., 2013). In the Orthoptera the Caelifera

27 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 Table 9. Scaling of sexual size dimorphism with body size in assorted genera of orthopteroid insects. In columns 5, 6 and 7 mean male and female body lengths (BL) and average SSD are given. Values in parentheses represent the respective ranges. In the last column, the slope (β) of the RMA regression of log10 (male BL) on log10 (femaleBL) and the 95% confidence intervals (in parentheses) are shown. In bold type, genera that follow Rensch’s rule or its converse. The extensive bibliography consulted for the construction of this Table is readily available from the corresponding author.

ORDER FAMILY GENUS N° OF MALE BL FEMALE BL BL SSD [F/M] βRMA TAXA Orthoptera Atractomorpha 21 20.0 30.2 1.52 0.997 (Caelifera) Saussure, 1862 (16.0-24.5) (24.0-36.0) (1.35-2.08) (0.80-1.27) Pamphagidae Acinipe Rambur, 1838 6 33.3 48.9 1.45 0.571 (29.0-41.0) (37.5-69.5) (1.29-1.70) (0.42-0.68) Pamphagidae Asiotmethis Uvarov, 7 27.5 35.5 1.29 1.064 1943 (25.0-31.5) (31.7-41.0) (1.20-1.36) (0.76-1.53) Acrididae Calliptamus Serville, 7 17.6 26.9 1.53 1.287 1831 (14.0-19.5) (22.5-29.0) (1.41-1.68) (0.84-2.34) Acrididae Sphingonotus Fieber, 12 17.6 24.5 1.39 0.941 1852 (13.5-22.0) (17.8-31.0) (1.16-1.70) (0.65-1.22) Acrididae Oedaleus Fieber, 33 26.2 34.7 1.32 0.897 1853 (19.0-38.2) (24.2-46.1) (1.10-2.04) (0.71-1.07) Acrididae Chorthippus Fieber, 99 15.4 20.5 1.34 0.981 1852 (10.0-24.0) (13.3-34.5) (1.07-1.58) (0.83-1.45) Acrididae Arcyptera Serville, 12 23.1 30.4 1.32 0.880 1838 (21.0-28.0) (25.5-35.5) (1.09-1.38) (0.40-1.68) Acrididae Dociostaurus Fieber, 10 15.3 22.3 1.46 0.902 1853 (9.0-23.0) (12.5-33.5) (1.30-1.86) (0.63-1.17) Acrididae Omocestus Serville, 17 13.1 16.9 1.29 0.851 1838 (10.3-17.2) (13.8-21.5) (1.12-1.41) (0.65-1.07) Acrididae Stenobothrus Fischer, 20 16.5 21.5 1.32 0.852 1853 (11.0-22.0) (14.5-34.0) (1.16-1.53) (0.67-1.13) Acrididae Melanoplus Stål, 1873 293 19.0 23.4 1.22 1.010 (9.5-33.0) (14.5-48.0) (0.84-1.82) (0.95-1.10) Acrididae Conophyma 78 14.9 19.4 1.30 0.858 Zubovski, 1898 (10.2-19.8) (13.1-27.6) (1.01-1.56) (0.76-0.97) Acrididae Pseudoceles Bolívar, 11 17.6 23.9 1.35 0.959 1899 (16.0-20.0) (21.0-27.0) (1.25-1.49) (0.62-1.67) Acrididae Thalpomena 9 16.5 22.9 1.39 1.190 Saussure, 1884 (14.5-18.5) (20.5-25.0) (1.22-1.56) (0.20-2.18) Acrididae Diexis Zubovski, 1899 8 13.2 21.9 1.65 0.702 (10.9-15.3) (17.8-27.5) (1.48-2.00) (0.32-1.11) Acrididae Oxya Serville, 1831 16 22.3 28.2 1.28 1.304 (17.7-29.8) (21.5-32.2) (1.04-1.58) (0.92-2.17) Dericorys Serville, 8 26.3 37.7 1.50 1.522 1838 (18.4-46.99 (26.5-53.4) (1.14-1.18) (1.06-2.03) Lentulidae Usambilla Sjöstedt, 12 7.7 9.3 1.21 0.956 1910 (7.0-8.3) (8.5-10.9) (1.13-1.39) (0.74-1.25) Romaleidae Xyleus Gistel, 1848 17 32.3 44.3 1.37 0.807 (29.2-36.4) (38.5-52.6) (0.67-0.80) (0.63-1.06) Romaleidae Zoniopoda Stål, 1873 10 32.3 43.0 1.33 1.025 (28.8-39.4) (36.0-48.9) (1.23-1.45) (0.63-1.46) Romaleidae Argiacris Walker, 11 33.9 52.9 1.54 0.440 1870 (29.8-37.6) (38.6-63.1) (1.14-1.85) (0.17-0.99)

28 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects

ORDER FAMILY GENUS N° OF MALE BL FEMALE BL BL SSD [F/M] βRMA TAXA Romaleidae Staleochlora Roberts 12 33.8 51.2 1.52 1.34 & Carbonell, 1992 (25.9-38.9) (43.7-58.7) (1.33-1.92) (-1.12-1.72)

Romaleidae Phaeoparia Stål, 1873 14 24.5 35.3 1.45 1.049 (15.6-32.2) (22.4-42.6) (1.30-1.56) (0.94-1.28)

Romaleidae Maculiparia Jago, 15 21-4 31.9 1.49 0.924 1980 (18-6-25.0) (27.8-38-2) (0.60-0.72) (0.65-1.45)

Romaleidae Taeniophora Stål, 11 14.4 18.4 1.27 0.919 1873 (11.9-16.9) (14.1-21-7) (1.19-1.33) (0.79-1.20)

Romaleidae Phrynotettix Glover, 10 27.7 38.7 1.41 1.154 1872 19-9-34.5) (28.6-47.0) (1.25-1.59) (0.83-1.61)

Orthoptera Tettigoniidae Isophya Brunner von 31 22.3 23.1 1.04 1.057 (Ensifera) Wattewyl, 1878 (16.5-31.5) (17.3-32.5) (0.90-1.30) (0.87-1.36)

Tettigoniidae Poecilimon Fischer, 55 17.9 19.7 1.10 0.949 1853 (12.5-28.8) (14-0-32.00) (0.93-1.63) (0.82-1.10)

Tettigoniidae Platycleis Fieber, 1853 37 18.2 19.6 1.08 1.010 (13.0-28.0) (14.5-30.3) (0.95-1.31) (0.89-1.20)

Tettigoniidae Metrioptera Wesmäel, 21 17.5 20.0 1.13 0.701 1838 (14.3-25.0) (15.5-34.0) (1.00-1.34) (0.61-0.96)

Tettigoniidae Pholidoptera 22 21.2 24.1 1.14 1.05 Wesmäel, 1838 (14.0-26.5) (18.0-31.0) (0.99-1.43) (0.74-1.41)

Tettigoniidae Eupholidoptera 13 22.0 23.8 1.04 0.85 Maran, 1953 (18.0-26.5) (18.0-28.5) (0.92-1.13) (0.30-1.12)

Tettigoniidae Rhacocleis Fieber, 11 18.6 21.0 1.13 0.706 1853 (14.5-22.1) (14.3-28.4) (0.98-1.28) (0.63-1.49)

Tettigoniidae Antaxius Brunner von 10 17.4 19.5 1.12 0.991 Wattenwyl, (14.5-19.5) (16.3-21.8) (1.02-1.32) (0.41-1.59)

Tettigoniidae Berthold, 16 25.6 27.5 1.08 0.958 1827 (21.0-34.5) (22.2-36.5) (0.98-1.19) )0.68-1.19)

Tettigoniidae Ephippigerida Bolivar, 10 26.8 28.5 1.07 1.054 1903 (15.3-46.5) (16.2-41.0) (0.94-1.17) (0.82-1.35)

Tettigoniidae Uromenus Bolívar, 25 25.4 26.8 1.06 0.937 1878 (18.3-36.0) (17.3-36.5) (0.85-1.19) (0.80-1.16)

Raphidiophoridae Dolichopoda Bolívar, 19 13.6 18.8 1.02 1.118 1880 (13.0-34.0) (13.0-31.5) (0.76-1.21) (0.83-1.42)

Gryllidae Eugryllodes Chopard, 13 13.9 13.5 0.97 0.711 1927 (12.0-17.0) (11.0-18.5) (0.87-1.12) (0.61-0.99)

Myrmecophilidae Mrmecophilus 9 3.0 3.4 1.11 0.897 Berthold, 1827 (2.2-4.5) (2.2-4.7) (1.00-1.34) (0.49-1.21)

Phasmatodea 10 58.2 75.3 1.34 1.591 Redtenbacher, 1908 (32.0-80.0) (60.0-98.0) (1.13.2.00) (1.04.2.35)

Diapheromeridae Candovia Stål, 1875 9 54.0 73.8 1.37 0.976 (41.0-79.0) (57-0-109.0) (1.20-1.56) (0.72-1.31)

Diapheromeridae Clonaria Stål, 1875 15 54.4 70.3 1.29 0.77 (35.0-68.0) (42.0-108.0) (0.87-1.71) (0.49.1.27)

Diapheromeridae Serville, 33 51.9 69.2 1-34 1.037 1838 (35.0-75.0) (42.5-90.0) (1.06-1.63) (0.91-1.21)

Diapheromeridae Brunner 24 59.4 81.6 1.38 0.959 von Wattenwyl, 1893 (48.0-85.0) (59.5-116.0) (1.12-2.03) (0.78-1.20)

Pseudophasmatidae Anisomorpha Gray, 11 34.1 48.7 1.46 1.046 1835 (24.0-46.5) (30.0-62.5) (1.04-2.16) (0.39-1.70)

29 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016

ORDER FAMILY GENUS N° OF MALE BL FEMALE BL BL SSD [F/M] βRMA TAXA Phasmatidae Phasma Lichtenstein, 14 49.1 70.2 1.44 1.320 1796 (38.0-59.0) (61.0-80.0) (1.29-1.84) (0.84-2.06) Phasmatidae Phobaeticus Brunner 11 139.4 241.3 1.69 0.533 von Wattenwyl, 1907 (118.1-165.5) (163.0-343.3) (1.30-2.56) (0.32-1.17) Phasmatidae Stål, 1875 10 75.5 101.9 1.35 0.81 (47.0-110.0) (54.0-165.0) (1.04-1.60) (0.74-1.38) Promachus Stål, 1875 16 44.3 65.0 1.46 0.86 (21.0-53.0) (29.0-88.0) (1.10-1.76) (0.52-0.97) Mantodea Mantidae Rhodomantis Gilgio- 8 45.5 61.5 1.35 0.840 Tos, 1917 (37.3-57.7) (50.8-81.5) (1.20-1.61) (-1.36-1.98) Mantidae Hierodula Burmeister, 10 64.8 72.6 1.12 0.945 1839 (52.0-83.5) (57.0-98.0) (1.01-1.17) (0.87-1.41) Hymenopodidae Oxypiloidea 12 21.2 26.2 1.23 0.649 Schulthess, 1898 (19.0-22.5) (22.0-35.0) (1.09-1.46) (0.33-0.96) Liturgusa Saussure, 20 22.8 29.4 1.29 0.698 1869 (18.7-30.7) (23.8-42.1) (1.14-1.63) (0.51-0.94) Blattodea Ischnoptera 14 15.2 13.5 0.89 1.033 Burmeister, 1838 (10.3-21.0) (9.3-19.0) (0.72-1.03) (0.76-1.56) Ectobiidae Ectobius Stephens, 24 8.3 7.6 0.92 1.037 1835 (6.3-10.5) (5.8-9.5) (0.75-1.17) (0.77-1.41) Ectobiidae Neoblattella Shelford, 10 11.6 12.4 1.07 0.955 1911 (9.2-14.2) (9.3-14.7) (0.89-1.30) (0.69-1.69) Ectobiidae Phyllodromica Fieber, 26 6.5 7.0 1.10 1.518 1853 (4.5-8.2) (5.7-8.5) (0.90-1.50) (1.14-2.46) Dermaptera Forficula Linnaeus, 22 11.2 10.6 0.95 1.085 1758 (7.5-15.5) (6.8-13.3) (0.78-1.31) (0.96-1.32) Labiduridae Forcipula Bolívar, 12 18.9 |8.8 0.99 1.019 1897 (13.5-25.5) (13.5-25.5) (0.81-1.18) (0.94-1.19) Mantophasmatodea several several 8 14.0 16.5 1.27 1.885 (9.4-23.6) (11.7-22.5) (1.01-1.54) (0.90-4.13) are generally more dimorphic than Ensifera: the length and those of the second species, 16.17 former average 1.37 SSD in body length ranging mm producing SSDs of 1.68 and 2.79 respec- from 0.83 to 2.45, while the latter show a mean tively (López et al., 2013) which largely exceeds SSD of 1.09 (0.77-1.44) (Hochkirch & Gröning, the range observed in many genera containing 2008). However, different families and subfami- large numbers of species (Table 9). lies within each suborder show marked differ- Very few studies of Rensch’s rule have been ences in degrees of SSD (Table 8). The same is performed in orthopteroid insects either at the true for different related genera (Table 9 and Bi- interspecific (Bidau et al., 2013) or intraspecific dau et al., 2013). Sometimes, extreme differenc- (Bidau & Martí, 2007a, 2008a, b) levels. From es in SSD occur in very closely related species Tables 8 and 9 it can be seen that the vast as is the case of two recently evolved species majority of orthopteroid taxa analyzed show of the pamphagid genus Purpuraria Enderlein isometric scaling of SSD with body size dem- from the Canary Islands that, despite their very onstrated by RMA slopes not different from 1. close relationship and morphological similarity, Of course, these results could be different if a show a dramatic difference in SSD: while Purpu- phylogenetic approach is used but compre- raria magna López & Oromi and Purpuraria erna hensive phylogenies for these groups are not Enderlein show females of similar size (average available. However, in a number of non-orthop- body lengths, 42.41 and 43.48 mm respective- teroid cases, SSD has been shown to lack phy- ly) males of the first species average 25.2 mm in logenetic signal and Rensch’s rule is not veri-

30 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects fied with or without the phylogenetic approach allometry and the allometric scaling is frequent- (e.g. Martínez & Bidau, 2014; Martínez et al., ly different in males and females (see Table 5). 2014) while in others hyperallometry has been Many examples are clear from our results: in unquestionably demonstrated (e.g. Frýdlová & Dichroplus pratensis which follows Rensch’s Frynta, 2015). At the intraspecific level, howev- rule independently of the character used for er, orthopteroids showed a variety of responses its testing, SSD for body length (1.33) is much when scaling of SSD was analyzed (Table 1). lower than that estimated for all other five lin- Only a fourth of the cases showed a response ear characters. This is a direct consequence consistent with Rensch’s rule (SSD decreas- of the different degrees of male and female al- ing with increasing body size) and interestingly lometry of these structures (allometric equations enough, 17% of the species showed the con- not shown in this paper; see Table 4 in Bidau verse trend which according to Rensch’s rule & Martí, 2008b). Dichroplus vittatus that also original formulation should be expected when showed a considerable variation in SSD for dif- males are larger, not smaller, than females. Fur- ferent characters, produced converse Rensch’s thermore, more than half the species displayed patterns in all cases except for pronotum length isometric scaling indicating that Rensch’s rule which is, significantly, a structure frequently is not a common pattern in orthopteroids at the used in orthopteroid insects as a proxy for body intraspecific level. In fact, these results suggest size. Conversely, Podisma sapporensis exhib- that the scaling of SSD with body size is a rather ited a converse pattern for pronotum length but idiosyncratic phenomenon in these insects with isometry for all other traits (see Table 4). Even each species following its particular trend. The the length of the third femur, also used frequent- latter is reflected in cases such as the five close- ly to estimate size in orthopteroid insects, can ly allied grasshopper species belonging to the produce discordant results: the four species of Dichroplini of the Melanoplinae (Dichrop- the romaleid genus Brachystola Scudder show lus fuscus, D. pratensis, D. vittatus, Ronderosia moderate (for the family) female-biased SSD for bergii, and Scotussa cliens) one of which fol- body length (1.1-1.2) and pronotum length (1.1- lows Rensch’s rule, two its converse and two, 1.3) but surprisingly (and uniquely) the larger isometric scaling (Table 1). Nevertheless, one females have shorter – in absolute length- hind thing seems to be true: it has been considered legs than males producing male-biased SSDs a precondition for Rensch’s rule that male size ranging from 0.77 to 0.88. However, allometries variability is higher than that of females (Fair- are not inevitable (Clutton-Brock et al., 1977) bairn, 1997) which was substantiated by our re- but when they occur differentially in both sexes sults. As a confirmation, in most species show- it is not unreasonable to infer different selective ing converse Rensch’s rule, females were more pressures on the same structure in males and variable in size than males while those species females. This is probably the case in to exam- with isometric scaling showed practically the ples described in the Results section. The dra- same degree of variability in both sexes. matic difference between the degree of SSD for However, this kind of results must be evalu- body length and SBCD for cerci (forceps) in ear- ated cautiously. This is because different char- wigs could be a result of the multiple functions acters used to evaluate SSD could yield dif- that these structures perform in males, such as: ferent estimations of dimorphism and produce male-male aggressive interactions, weapons, discordant scaling patterns, thus the election sexual display, and clasping of females (Brice- of such characters is of utmost relevance (Fair- ño & Eberhard, 1995). In the other example, bairn, 2007; Fox et al., 2015). In insects, body that of the bark of the genus Liturgusa mass data are hard to come by, so that in most (Svenson, 2014) femurs of the forelegs show cases, size and SSD are analyzed using linear a degree of sexual dimorphism comparable to measurements of body length or other body that of body length, which largely exceeds that structures such as legs, wings, pronotum, head, of the femurs of meso- and metathoracic legs, etc. The election of such a character would not and also exhibit differential allometry respect to be problematic if the length of these different body length. It is worth noting that size of fore- structures scaled isometrically with general size leg femurs and tibiae are essential in determin- but this is rarely the case: most structures show ing optimum prey size in mantids (Holling et al.,

31 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 1976). Interestingly in this genus, a converse species with large geographic distributions. Rensch pattern is obtained when using body The effects of external conditions on adult length and prothoracic femur length as estima- body size and SSD of orthopteroid insects have tors of body size, while sexual dimorphism for been extensively studied experimentally. Again, second and third femur length and pronotum as shown by the examples summarized in table length display sexual isometry. 6 responses to variation in living conditions, diet, Latitudinal, elevational, and longitudinal size temperature, etc. are largely idiosyncratic. In- clines related to variation in biotic and abiotic crease or decrease of body size may be accom- factors are frequent in insects and have been panied by different and contrasting responses of relatively well studied in orthopteroid insects. SSD. For example, the effects of crowding may The most frequent pattern is one in which body produce increased SSD (e.g. Ornithacris turbida), size decreases towards higher latitudes or el- decreased size and SSD (e.g. Schistocerca pal- evations (the converse Bergmann’s rule) and it lens, Melanoplus differentialis (Thomas), and dif- is most satisfactorily explained by a shortening ferent strains of Locusta migratoria), while no size of the developmental time as seasonality in- or SSD changes were observed in similar experi- creases and temperature decreases. Because ments with the common cricket Acheta domesti- SSD has been also shown to vary geographi- cus. These and other experiments with varying liv- cally in many species, it has been suggested ing conditions strongly suggest species-specific that Bergmann’s (or converse Bergamnn’s) rule responses of body size to external factors which, and Rensch´s rule may overlap in the analysis of if translated to nature could explain the diversity body size variation (Blanckenhorn et al., 2006; of SSD patterns observed in orthopteroid insects. Bidau & Martí, 2007a). The possible correlation Furthermore, while estimations of SSD are usually is a logical one since Rensch’s rule depends performed at the adult stage, external factors act on body size which in turn shows geographic during the whole period of development. One of clinal variation. The majority of species shown in the proximate causes that have been invoked to Table 1 presented clinal patterns of geographic explain size differences between males and fe- body size variation mainly of the converse Berg- males in insects is the higher number of larval in- mannian type. In most cases, body size varia- stars shown by females of most species (Esperk tion is accompanied by a corresponding clinal et al., 2007). Although this phenomenon occurs change in the degree of SSD along the same frequently in orthopteroid insects (see Table 7), it spatial coordinates. In some cases (e.g. Dichro- cannot be the sole cause of female-biased SSD. plus pratensis and D. vittatus) that show strong For example, both giant weta Deinacrida spe- latitudinal and altitudinal patterns this correla- cies and the pyrgomorphid Phymateus leprosus tion, although expected, was not found but this showh high female-biased SSD but equal num- is due to confounding effects of elevation within ber of instars for both sexes, and in the praying the latitudinal patterns that span many degrees mantis Pseudomantis albofimbriata males, not of latitude (Bidau & Martí, 2008b). females, undergo an additional nymphal stage Since in most insects larger sizes occur in (Table 7). The problem is further complicated in more favorable conditions, an explanation of that most species do not show significant SSD Rensch’s rule and its converse could be pro- until the more advanced developmental stages or duced if we assume differential sensitivity of even only after the final moult (Stilwell et al., 2010; males and females to environmental factors as Table 7). Furthermore, other factors such as size suggested by Teder &Tammaru (2005). at hatching, growth rate, size-dependent survival, If females are more sensitive, as conditions and phenotypic plasticity of the characters under improve, they could achieve their optimal size study greatly influence adult SSD (Stilwell et al., more readily than in poorer conditions produc- 2010). Sex differences in plasticity resulting from ing an increase in SSD (converse Rensch’s rule). varying degrees of stabilizing and directional se- The reverse would occur if males are the most lection on body size or the size of specific char- sensitive sex. Thus, in this hypothetical scenario acters, are probably the source of much of the Rensch’s rule and its converse (not SSD per se) observed variation of SSD and is a promising field would be subproducts of body size variations of study to start disentagling the proximate and related to environmental conditions, specially in ultimate causes of SSD (Stilwell et al., 2010).

32 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects CONCLUSIONS LITERATURE CITED

ABOUHEIF, E. & D. J. FAIRBAIRN. 1997. A comparative analy- 1. Orthopteroid insects show several different sis of sexual size dimorphism: assessing Rensch’s rule. scaling patterns of SSD with body size and this American Naturalist 149: 540-562. ADIS J., C. F. SPERBER, E. G. BREDE, S. CAPELLO, M. C. is expressed at intra and interspecific levels. FRANCESCHINI, M. HILL & P. POLAR. 2008. Morphomet- 2. Scaling patterns may differ significantly ric differences in the grasshopper Cornops aquaticum (Bruner, 1906) from South America and South Africa. Jour- within taxa depending on the body size estima- nal of Orthoptera Research 17: 141-147. tors considered for analysis and even closely ALLEN, L. E., K. L. BARRY & G. I. HOLWELL. 2013. Different related species may show completely contrast- paths to sexual dimorphism in two praying mantids, Pseu- domantis albofimbriata and Hierodula majuscula. Insect ing patterns. Science 21: 227-233. 3. Rensch’s rule is just one of the possible ANDERSSON, M. 1994. Sexual selection. Princeton University Press, Princeton. modes of scaling of SSD with body size and it ANTONIOU, A. 1973. The life history of the grasshopper Or- can hardly be regarded as a proper “rule”. nithacris turbida (Walker) (Orthoptera; Acrididae; Cyrta- 4. Numerous environmental factors affect canthacridinae) in the laboratory. Journal of Natural His- tory 7: 461-469. SSD both in nature and experimental studies ANTONIOU, A. & C. J. ROBINSON. 1974. Laboratory studies suggesting the role of differential plasticity be- on the effect of crowding on phase and the life history of Schistocerca pallens (Thunberg) (Orthoptera: Acrididae: tween males and females in shaping SSD and Cyrtacanthacridinae). Journal of Natural History 8: 701-715. its variation. ASHBY, P. D. 1997. Conservation of mass-specific metabolic rate among high-and low-elevation populations of the acri- 5. The study of plasticity and the comparison did grasshopper Xanthippus corallipes. Physiological and of sexual dimorphism for different characters Biochemical Zoology 70: 701-711. that may be under different selective pressures BAMIDELE, A. O. & W. A. MUSE. 2012. A morphometric study of the variegated grasshopper (Linn.) (Orthoptera: Pyrgo- are needed in the future for an understanding of morphidae) from parts of Southern Nigeria. Ife Journal of the proximate and ultimate causes of SSD. Science 14: 61-73. BARENBLATT, G. 2003. Scaling. Cambridge University Press, General conclusion: Despite the pervasive Cambridge. nature of sexual size dimorphism and the enor- BECCALONI, G. W. 2015. Cockroach Species File Online. mous wealth of studies devoted to understand Version 5.0/5.0. World Wide Web electronic publication. [June 2015] its evolutionary significance and the mecha- BELL, W. J., L. M. ROTH & C. A. NALEPA. 2007. Cockroaches: nisms responsible for its enormous variation ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore. among widely different organisms as shown in BERGMANN, C. 1847. Über die Verhätlnisse der Warmeökono- this paper, we still remain confronted with the mie der Thiere zu ihrer Grösse. Göttinger Studien 1: 595-708. enigma of inter-sex size differences. One of the BERNER, D. & W. U. BLANCKENHORN. 2006. Grasshopper ontogeny in relation to time constraints: adaptive diver- multiple intriguing problems is the relationship gence and stasis. Journal of Animal Ecology 75: 130-139. between SSD and body size and why in com- BIDAU, C. J. 2014. Patterns in Orthoptera . I. Ad- aptations in ecological and evolutionary contexts. Journal parative studies, the latter usually shows strong of Insect Biodiversity 2 (20): 1-39. phylogenetic signal while SSD usually does not. BIDAU, C. J. & D. A. MARTÍ. 2007a. Clinal variation of body This may in part reflect the fact that SSD is not a size in Dichroplus pratensis (Orthoptera: Acrididae): in- version of Bergmann’s and Rensch’s rules. Annals of the classic organismal property such as body mass Entomological Society of America 100: 850-860. or form, but an adimensional measurement of BIDAU, C. J. & D. A. MARTÍ. 2007b. Dichroplus vittatus (Acri- didae, Melanoplinae) follows the converse to Bergmann’s a difference. This special characteristic of SSD rule. Bulletin of Entomological Research 97: 69-79. strongly suggests that novel methods for its BIDAU, C. J. & D. A. MARTÍ. 2008a. Rensch’s rule in Dichrop- lus pratensis: a reply to Wolak. Annals of the Entomologi- study must be developed in the future. cal Society of America 101: 802-803. BIDAU, C. J. & D. A. MARTÍ. 2008b. Contrasting patterns of ACKNOWLEDGMENTS sexual size dimorphism in the grashoppers Dichroplus vit- tatus and D pratensis (Acrididae, Melanoplinae). Journal of Orthoptera Research 17: 201-211. This paper honors Prof. Dr. Axel O. Bach- BIDAU, C. J., D. A. MARTI & E. R. CASTILLO. 2013. Rensch’s rule is not verified in melanopline grasshoppers. Journal of mann, superb entomologist and excellent Insect Biodiversity 1(12): 1-14. teacher on the occasion of his 89th birthday. BIDAU, C. J., C. I. MIÑO, E. R. CASTILLO & D. A. MARTÍ. Alberto Taffarel and Elio Rodrigo Castillo ac- 2012. Effects of abiotic factors on the geographic distri- bution of body size variation and chromosomal polymor- knowledge the continuous support of CONICET phisms in two Neotropical grasshopper species (Dichro- (Argentina). We are grateful to two anonymous plus: Melanoplinae: Acrididae). In: Savopoulou-Soultani M., N.T. Papadopoulos, P. Milonas & P. Moyal (eds.), Abi- reviewers and the section editor for suggestions otic factors and insect abundance. Psyche (special issue) that improved the original manuscript. 2012, pp. 1-11 (article ID 863947).

33 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 BIGNELL, D. E., Y. ROISIN & N. LO. 2011. Biology of termites: CLUTTON-BROCK, T. 2010. We do not need a sexual selec- a modern synthesis. Springer Science, New York, 576 pp. tion 2.0-nor a theory of genial selection. Animal Behavior BJÖRKMAN, C., K. GOTTHARD & M. W. PETTERSONN. 2009. 79: e7-e10. Body size. In: Resh V. H. & R. T. Cardé (eds.), Encyclope- CLUTTON-BROCK, T. H., P. H. HARVEY & B. RUDDER. 1977. dia of Insects. 2nd Ed. Academic Press-Elsevier, Burling- Sexual dimorphism, socionomic sex ratio and body weight ton, pp. 114-116. in primates. Nature 269: 797-800. BLANCKENHORN, W. U. 2005. Behavioral causes and conse- CUNNINGHAM, J. T. 1900. Sexual dimorphism in the animal quences of sexual size dimorphism. Ethology 111: 977-1016. kingdom: A Theory of the evolution of secondary sexual BLANCKENHORN, W. U., R. C. STILLWELL, K. A. YOUNG, C. characters. Adam and Charles Black, London, 317 pp. W. FOX &K. G. ASHTON. 2006. When Rensch meets Berg- DARWIN, C. 1871. The Descent of man and selection in rela- mann, does sexual size dimorphism change with latitude? tion to sex. John Murray, London, 822 pp. Evolution 60: 2004–2011. DINGLE, H. & J. B. HASKELL. 1967. Phase polymorphism in BLANCKENHORN W. U., A. F. G. DIXON, D. J. FAIRBAIRN, M. the grasshopper Melanoplus differentialis. Science 155 W. FOELLMER, P. GIBERT, K. VAN DER LINDE, R. MEIER, S. (3762): 590-592. NYLIN, S. PITNICK, C. SCHOFF, M. SIGNORELLI, T. TEDER & EADES, D. C., D. OTTE, M. M. CIGLIANO & H. BRAUN H. C. WIKLUND. 2007a. Proximate causes of Rensch’s rule, does 2015. Orthoptera Species File. Version 5.0/5.0. [June sexual size dimorphism in result from sex differenc- 2015]. es in development time? American Naturalist 169: 245–257. ELLERS, O. 2001. Size matters. Complexity 6: 23-26. BLANCKENHORN, W. U., R. MEIER & T. TEDER. 2007b. ESPERK, T., T. TAMMARU, S. NYLIN & T. TEDER T. 2007. Rensch’s rule in insects, patterns among and within species. Achieving high sexualsize dimorphism in insects: females In: Fairbairn D. J., W. U. Blackenhorn & T. Székely (eds.), add instars. Ecological Entomology 3: 243–256. Sex, size and gender roles evolutionary studies of sexual EWELEIT, L. & K. REINHOLD. 2014. Body size and elevation: size dimorphism. Oxford University Press, Oxford, pp. 60-70. do Bergmann’s and Rensch’s rule apply in the polytypic BOHONAK, A. J. & K. VAN DER LINDE. 2004. RMA: Soft- bushcricket Poecilimon veluchianus? Ecological Entomol- ware for Reduced Major Axis regression. Java version. ogy 39: 133-136. http://www.kimvdlinde.com/professional/rma.html FABRICIUSOVÁ, V., P. KAŇUCz & A. KRIŠTÍN. 2008. Body size BRICEÑO, R. D. & W. G. EBERHARD. 1995. The functional patterns of Pholidoptera frivaldskyi (Orthoptera) in very isolat- morphology of male cerci and associated characters in ed populations. Journal of Orthoptera Research 17: 171-176. 13 species of tropical earwigs (Dermaptera: Forficulidae, FAIRBAIRN, D. J. 1997. Allometry for sexual size dimorphism: Labiidiae, Carcinophoridae, ). Smithsonso- pattern and process in the coevolution of body size in nian Contributions to Zoology 555: 1- 63. males and females. Annual Review of Ecology and Sys- BROCK, P. D. & J. W. HASENPUSCH. 2009. The Complete tematics 28: 659-687. Field Guide to Stick and Leaf Insects of Australia. CSIRO, FAIRBAIRN, D. J. 2007. Introduction: the enigma of sexual Collingswood, 216 pp. size dimorphism. In: Fairbairn D.J., W. U. Blanckenhorn BROCK, P. D. 2015. Phasmida Species File Online. Ver- & T. Székely (eds.), Sex, size and gender roles: Evolution- sion5.0/5.0. [June 2015]. http://Phasmida.SpeciesFile.org>. ary studies of sexual size dimorphism. Oxford University BROUGHMAN, J. W. 2014. Speciation and sexual selection. In: Press, Oxford, pp. 1-12. Losos J. B. (ed.), The Princeton guide to evolution, Princ- FAIRBAIRN, D. J. 2013. Odd Couples: Extraordinary differ- eton University Press, Princeton and Oxford, pp. 520-528. ences between the sexes in the animal kingdom. Princ- BROWN, J. H. & G. B. WEST. 2005. The origin of allometric scal- eton University Press, Princeton. ing laws in biology from genomes to ecosystems: towards a FAIRBAIRN, D. J., W. U. BLANCKENHORN & T. SZÉKELY T. quantitative unifying theory of biological structure and orga- 2007. Sex, size and gender roles: Evolutionary studies of nization. Journal of Experimental Biology 208: 1575-1792. sexual size dimorphism. Oxford University Press, Oxford. BUTLIN, R. K. & G. M. HEWITT. 1985. A hybrid zone between FORREST, T. G. 1987. Insect size tactics and developmental Chorthippus parallelus parallelus and Chorthippus paralle- strategies. Oecologia 73(2): 178-184. lus erythropus (Orthoptera: Acrididae): behavioural charac- FOX, G. A., A. M. COOPER & W. K. HAYES. 2015. The dilemma ters. Biological Journal of the Linnean Society 26: 287-299. of choosing a reference character for measuring sexual CALDER, W. A. 1996. Size, function, and life history. Dover, New York. size dimorphism, sexual body component dimorphism, and CARRANZA, J. 2009. Defining sexual selection as sex-depen- character scaling: cryptic dimorphism and allometry in the dent selection. Animal Behavior 77: 749-751. scorpion Hadrurus arizonensis. PLoS ONE 10 (3): e0120392. CEPEDA-PIZARRO, C., S. VEGA, H. VÁSQUEZ & M. EL- FRÝDLOVÁ, P. & D. FRYNTA. 2015. Strong support for GUETA. 2003. Morphometry and sexual dimorphism of Rensch’s rule in an American clade of lizards (Teiidae and Elasmoderus wagenknechti (Liebermann) (Orthoptera: Gymnophtalmidae) and a paradox of the largest tejus. The Tristiridae) in two population outbreaks. Revista Chilena Science of Nature 102: 1-11. de Historia Natural 76: 417-435. GASTON, K. J. 1991. Body size and probability of description: the CHAPPELL, E. M. 2008. Morphology, Phylogeography and beetle fauna of Britain. Ecological Entomology 16: 505-508. Drumming Behaviour of a New Zealand Ground Weta, GROETERS, F. R. & D. D. SHAW. 1996. Evidence for asso- Hemiandrus pallitarsis. MSC Thesis, Massey University, ciation of chromosomal form and development time from Palmerston North, New Zealand, 126 pp. complex clines and geographic races in the grasshopper CHOWN, S. L. & K. J. GASTON. 2010. Body size variation Caledia captiva (Orthoptera: Acrididae). Biological Jour- in insects: a macroecological perspective. Biological Re- nal of the Linnean Society 59: 243-259. views 85: 139-169. GWYNNE, D. T. 1984. Sexual selection and sexual diferences CHOWN, S. L. & K. J. GASTON. 2013. Macroecological pat- in Mormon Crickets (Orthoptera: Tettigoniidae, Anabrus terns in insect body size. In: Smith F. A. & Lyons S. K. (eds.), simplex). Evolution 38: 1011-1022. Animal body size: linking pattern and process across HARRIS, R., P. MCQUILLAN & L. HUGHES. 2012. Patterns space, time, and taxonomic group.The University of Chi- in body size and melanism along a latitudinal cline in the cago Press, Chicago, pp. 13-61. wingless grasshopper, Phaulacridium vittatum. Journal of CIPLAK, B., D. SIRIN, M. S. TAYLAN & S. KAYA. 2008. Altitu- Biogeography 39: 1450-1461. dinal size clines, species richness and population den- HASSALL, M. & F. W. L. GRAYSON. 1987. The occurrence sity: case studies in Orthoptera. Journal of Orthoptera of an additional instar in the development of Chorthippus Research 17: 157-163. brunneus (Orthoptera: Gomphocerinae). Journal of Natu- CLUTTON-BROCK, T. 2009. Sexual selection in females. Ani- ral History 21: 329-337. mal Behavior.77: 2–11. HIGAKI, M. & Y. ANDO. 2002. The effect of temperature on em-

34 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects bryonic development and local adaptation in the life cycle of Oikos 124: 610-619. Eobiana engelhardti subtropica Bey-Bienko (Orthoptera: Tet- LINDENFORS, P., J. L. GITTLEMAN & K. E. JONES K. E. 2007. tigoniidae). Applied Entomology and Zoology 37: 625-636. Sexual size dimorphismin mammals. In: Fairbairn D. I., W. HOCHKIRCH, A. & J. GRÖNING. 2008. Sexual size dimor- U. Blanckenhorn & T. Székely (eds.), Sex, size and gender phism in Orthoptera (sens. Str.): a review. Journal of Or- roles. Evolutionary studies of sexual size dimorphism. Ox- thoptera Research 17: 189–196. ford University Press, Oxford, pp. 16-26. HOLLING, C. S., R. L. DUNBRACK & L. M. DILL. 1976. Preda- LÓPEZ, H., D. HERNÁNDEZ-TEIXIDOR, N. MACÍAS- tor size and prey size: presumed relationship inthe mantid HERNÁNDEZ, C. JUAN & P. OROMI. 2013. A taxonomic Hierodula coarctata Saussure. Canadian Journal of Zool- revision and species delimitation of the genus Purpuraria ogy 54: 1760-1764. Enderlein, 1929 (Orthoptera: Pamphagidae) using an inte- HOLMA, F. 2009. Latitudinal Patterns in Body Size of Roesel’s grative approach. Journal of Zoological Systematics and Bush Cricket Metrioptera roeselii within and outside the Evolutionary Research 51: 176-183. Continuous Area of its Distribution. MSc Thesis, Sveriges LUONG-SKOVMAND, M. H. & G. BALANÇA. 1999. Bryophy- lantbruksuniversitet, Uppsala, Sweden, 23 pp. ma debilis (Karsch, 1896) nymphal instars (Orthoptera, HONEK, A. 1993. Intraspecific variation in body size and fecun- Acrididae, Cyrtacanthacridinae). Journal of Orthoptera dity in insects — a general relationship. Oikos 66: 483-492. Research 8: 110-118. HOPKINS, H., M. D. MAEHR, F. HAAS F. & L. S. DEEM. 2015. MARTÍNEZ, P. A. & C. J. BIDAU. 2016. Are-assessment of Dermaptera Species File. Version5.0/5.0. [June 2015]. Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Cte- . nomys) using a phylogenetic approach. Mammalian Biol- HOPPELER, H. & E. R. WEIBEL. 2005. Scaling functions to ogy: 81: 67-72. body size: theories and facts. Journal of Experimental Bi- MARTÍNEZ, P. A., T. FERREIRA AMADO & C. J. BIDAU C.J. ology 208: 1573-1574. 2014. A phylogenetic approach to the study of sexual size HOSTE, B., S. J. SIMPSON, S. TANAKA S., A. DE LOOF & M. dimorphism in Felidae and an assessment of Rensch’s BREUER. 2002. A comparison of phase-related shifts in rule. Ecosistemas 23: 27-36. behavior and morphometrics of an albino strain, deficient MASAKI, S. 1967. Geographic variation and climatic adaptation in in [His 7]-corazonin, and a normally colored Locusta mi- a field cricket (Orthoptera: Gryllidae). Evolution 21: 725-741. gratoria strain. Journal of Insect Physiology 48: 791-801. MASAKI, S. 1978. Climatic adaptation and species status in the HU, Y., F. ZHU, X. WANG & C. LE. 2011. Development time lawn ground cricket. II. Body size. Oecologia 35: 343-356. and body size in Eupolyphaga sinensis along a latitudinal MATSURA, T., T. INOUE & Y. HOSOMI. 1975. Ecological stud- gradient from China. Environmental Entomology 40: 1-7. ies of a mantid, Paratenodera angustipennis de Saussure HUBBELL, T. H. 1960. The sibling species of the Alutacea I. Evaluation of the feeding condition in natural habitats. Group of the bird-locust genus Schistocerca (Orthoptera, Research in Population Ecology 17: 64-76. Acrididae, Cyrtacanthacridinae). Miscellaneous Publica- MATSUURA, K. 2006. Early emergence of males in the termite tions of the Museum of Zoology of the University of Michi- Reticulitermes speratus (Isoptera: Rhinotermitidae): pro- gan 116: 1-142. tandry as a side effect of sexual size dimorphism. Annals HUIZENGA, K. M., M. D. SHAIDLE, J. S. BRINTON, L. N. A. of the Entomological Society of America 99: 625-628. GORE, M-A. EBO, A. J. SOLLIDAY & S. A. JULIANO. 2008. MAXWELL, M. R. 2014. Developmental patterns in Stagmo- Geographic differences in the body sizes of adult Romalea mantis limbata (Mantodea: Mantidae): variation in instar microptera. Journal of Orthoptera Research 17: 135-139. number, growth, and body size. Journal of Orthoptera Re- HUXLEY, J. 1932. Problems of relative growth. Methuen, London. search 23: 49-58. ISAAC, J. L. 2005. Potential causes and life-history conse- MCFARLANE, J. E. 1962. A comparison of the growth of the quences of sexual size dimorphism in mammals. Mammal house cricket (Orthoptera: Gryllidae) reared singly and in Review 35: 101–115. groups. Canadian Journal of Zoology 40: 559-560. JAGO, N. D. 1963. Some observations on the life cycle of Ey- MIÑO, C. I., C. N. GARDENAL & C. J. BIDAU. 2011- Small prepocnemis plorans meridionalis Uvarov, 1921 with a key scale variation within a mosaic hybrid zone of Dichroplus for the separation of instars at any stage. Procedings of the pratensis (Acrididae). Journal of Heredity 102: 184-195. Royal Entomological Society of London (A) 38: 113-124. MORBEY, Y. E. & R. C. YDENBERG. 2001. Protandrous ar- KEVAN D. K. MCE. & S. K. LEE. 1974. Atractomorpha sinen- rival timing to breeding areas: a review. Ecology Letters sis sinensis Bolívar (Orthoptera: Pyrgomorphidae) and its 4: 663-673. nymphal stages. Oriental Studies 8: 337-364. MORGAN, T. H. 1919. The genetic and operative evidence KOHLER, G., S. ROTH & K. REINHARD. 2008. Ten instars in the relating to secondary sexual characters. The Carnegie In- leprous grasshopper, Phymateus leprosus (Fabricius, 1793) stitution of Washington, Washington D.C. (Caelifera: Pyrgomorphidae): maximum number recorded NASRECKI, P. 2004. Orthoptera (grasshoppers, crickets, and in the . Bonner Zoologische Beitrage 56: 17-24. katydids).In: Evans A. V., R. W. Garrison & N. Schlager KOKKO, K., M. D. JENNIONS & R. BROOKS. 2006. Unifying (eds.), Grzymek’s animal life encyclopedia. 2nd Edit. Vol. 3. and testing models of sexual selection. Annual Review of Insects Thomson-Gale, Detroit, pp. 201-216. Ecology, Evolution and Systematics 37: 43-66. ORR, M. R. 1996. Life-history adaptation and reproductive iso- LABARBERA, M. 1986. The evolution and ecology of body lation in a grasshopper hybrid zone. Evolution 50: 704-716. size. In: Raup D. M. & D. Jablonski (eds.), Patterns and OTTE, D., L. SPEARMAN & M. B. D. STIEWE. 2015. Man- processes in the history of life. Springer, Berlin, pp. 69-98. todea Species File Online. Version 5.0/5.0. [June 2015]. LABARBERA, M. 1989. Analyzing body size as a factor in . ecology and evolution. Annual Review of Ecology and PARSONS, S. M. & A. JOERN. 2014. Life history traits associ- Systematics 20: 92-117. ated with body size covary along a latitudinal gradient in a LAIOLO, P., J. C. ILLERA & J. R. OBESO. 2013. Local climate generalist grasshopper. Oecologia 174: 379-391. determines intra‐and interspecific variation in sexual size PRETE, F. R., H. WELLS, P. H. WELLS & L. E. HURD. 1999. The pray- dimorphism in mountain grasshopper communities. Jour- ing mantids. The Johns Hopkins University Press, Baltimore. nal of Evolutionary Biology 26: 2171-2183. PRICE, P. W., R. F. DENNO, M. D. EUBANKS, D. L. FINKE & I. LEHMANN, G. U. & A. W. LEHMANN. 2008. Variation in body KAPLAN. 2011. Insect ecology. behavior, populations and size among populations of the bushcricket Poecilimon communities. Cambridge University Press, Cambridge. thessalicus (Orthoptera: Phaneropteridae): an ecological RANGEL, T. F., J. A. F. DINIZ-FILHO & L-M. BINI. 2010. SAM: adaptation. Journal of Orthoptera Research 17: 165-169. Acomprehensive application for spatial analysis in macro- LEVY, R. A. & C. R. NUFIO. 2014. Dispersal potential impacts ecology. Ecography 33: 1-5. size clines of grasshoppers across an elevation gradient. REEVE, J. P. & D. J. FAIRBAIRN. 1999. Change in sexual size

35 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 dimorphism as a correlated response to selection on fe- typic plasticity. Oikos 118: 703-712. cundity. Heredity 83: 697-706. STILWELL, R. C., W. U. BLANCKENHORN, T. TEDER, G. DA- REINHARD, J. 2007. Adult Size in Insects: Developmental VIDOWITZ & C.W. FOX. 2010. Sex differences in pheno- Responses to Temperature of the German Cockroach Bla- typic plasticity affect variation in sexual size dimorphism tella germanica and the Large Milkweed Bug Oncopeltus in insects: from physiology to evolution. Annual Review of fasciatus. BSc Thesis, University of Edinburgh, Scotland. Entomology 55: 227-245. REISS, M. J. 1986. Sexual dimorphism in body size: are larger SVENSON, G. J. 2014. Revision of the Neotropical bark man- species more dimorphic? Journal of Theoretical Biology tis genus Liturgusa Saussure, 1869 (Insecta, Mantodea, 121: 163-172. Liturgusini). ZooKeys 390: 1-214. Reiss, M. J. 1989.The allometry of growth and reproduction. SWORD, G. A. & R. F. CHAPMAN. 1994. Monophagy in a po- Cambridge University Press, Cambridge. lyphagous grasshopper, Schistocerca shoshone. Entomo- RENSCH, B. 1950. Die abhangigkeit der relativen sexual dif- logia Experimentalis et Applicata 73: 255-264. ferenz von der korpengrösse. Bonner Zoologische Be- TAMMARU, T., T. ESPERK, V. IVANOV & T. TEDER. 2010. itrage 1: 58-69. Proximate sourcesof sexual size dimorphism in insects: RENSCH, B. 1960. Evolution above the species level. Colum- locating constraints on larvalgrowth schedules. Evolution- bia University Press, New York. ary Ecology 24: 161–175. RICHARDS, A. M. 1973. A comparative study of the biology TATSUTA, H. & S. AKIMOTO. 1998. Sexual differences in the of the giant wetas Deinacrida heterocantha and D. fallai pattern of spatial variation in the brachypterous grasshop- (Orthoptera: Henicidae) from New Zealand. Journal of Zo- per Podisma sapporensis (Orthoptera: Podisminae).Ca- ology 169: 195-236. nadian Journal of Zoology 76: 1450-1455. RITCHIE, J. M. 1981. A taxonomic revision of the genus Oe- TEDER, T. 2014. Sexual size dimorphism requires a corre- daleus Fieber (Orthoptera: Acrididae). Bulletin of the Brit- sponding sex difference in development time: a meta- ish Museum (Natural History) (Entomology) 42: 83-183. analysis ininsects. Functional Ecology 28: 479-486. ROFF, D. A. & T. MOUSSEAU. 2005. The evolution of the pheno- TEDER, T. & T. TAMMARU. 2005. Sexual size dimorphism typic covariance matrix: evidence for selection and drift in within species increases with body size in insects. Oikos Melanoplus Journal of Evolutionary Biology 18: 1104-1114. 108: 321–334. ROMERO, M. L., N. ROSETTI & M. I. REMIS 2014. Morpho- THOMPSON, D. W. 1917. On growth and form. Cambridge metric variation affecting sexual size dimorphism in University Press, Cambridge, 1140 pp. Neopedies brunneri (Orthoptera: Acrididae). Annals of the THORNE, B. L. 1983. Alate production and sex ratio in colo- Entomological Society of America 107: 257-263. nies of the Neotropical termite Nasutitermes corniger SAN MARTÍN Y GOMEZ, G. S. & H. VAN DYCK. 2012. Eco- (Isoptera; Termitidae). Oecologia 58: 103-109. typic differentiation between urban and rural populations WALLACE, A. R. 1889. Darwinism. An exposition of the theory of the grasshopper Chorthippus brunneus relative to cli- of natural selection, with some of its applications. Macmil- mate and habitat fragmentation. Oecologia 169: 125-133. lan, London. SCHMIDT-NIELSEN, K. 1975. Scaling in biology: the conse- WASON, E. L. & S. C. PENNINGS. 2008. Grasshopper (Or- quences of size. Journal of Experimental Zoology 194: thoptera: Tettigoniidae) species composition and size 287-397. across latitude in Atlantic coast salt marshes. Estuaries SCHMIDT-NIELSEN, K. 1984. Scaling: why is animal size so and coasts 31: 335-343. important. Cambridge University Press, Cambridge. WEBB, T. J. & R. P. FRECKLETON. 2007. Only half right: spe- SHINE, R. 1989. Ecological causes for the evolution of sexual cies with female-biased sexual size dimorphism consis- dimorphism: a review of the evidence. Quarterly Review of tently break Rensch’s rule. PLoSONE 8: e897. Biology 64: 419-461. WEDELL, N. 1997. Ejaculate size in bushcrickets: the impor- SIVINSKI, J. 1978. Intrasexual aggression in the stick insects tance of being large. Journal of Evolutionary Biology 10: veliei and D. covilleae and sexual dimor- 315-325. phism in the Phasmatodea. Psyche 85: 395-405. WHITMAN, D. G. 2008. The significance of body size in the SMITH, F. A. & S. K. LYONS. 2013. Animal body size: linking Orthoptera, a review. Journal of Orthoptera Research 17: pattern and process across space, time and taxonomic 117–134. group. University of Chicago Press, Chicago. WILLOTT, S. J. & M. HASSALL. 1998. Life‐history responses SNELL, O. 1892. Die abhängigkeit des hirngewichts von dem of British grasshoppers (Orthoptera: Acrididae) to temper- körpergewicht und den geistigen fähigkeiten. Archives für ature change. Functional Ecology 12: 232-241. Psychiatrie 23: 436–446. ZENG, Y. & D. H. ZHU. 2014. Geographical variation in body STILLWELL, R. C. & C. W. FOX 2009. Geographic variation size, development time, and wing dimorphism in the crick- in body size, sexual size dimorphism and fitness compo- et Velarifictorus micado (Orthoptera: Gryllidae). Annals of nents of a seed beetle: local adaptation versus pheno- the Entomological Society of America 107: 1066-1071.

36