Translator Disclaimer
1 July 2014 Developmental Patterns in Stagmomantis limbata (Mantodea: Mantidae): Variation in Instar Number, Growth, and Body Size
Author Affiliations +
Abstract

Development affects many components of life history and fitness, including body size. The present study examined the influence of developmental pattern, specifically the number of nymphal instars, on body size (pronotum length) in the praying mantid Stagmomantis limbata Hahn. Mantids were reared in the laboratory from hatching, on standardized diet, to examine variation in instar number. These lab data were then used to assess developmental patterns forfield-collected female nymphs. Laboratoryreared males and females varied in number of instars. Most females required 6 nymphal instars to reach adulthood (64%), whereas 36% underwent 7 instars. Seven-instar females reached the 4th, 5 th, and 6th instars faster than six-instar females, but had shorter pronota than the six-instar females at each of these stages. Seven-instar females were longer than six-instar females at adulthood. Interestingly, the total developmental period from hatching to adulthood was similar for lab-reared seven-instar and six-instar females. In the lab, most males (91%) underwent 6 instars, with the remaining 9% following a five-instar pattern. By the 4th instar, differences between the sexes began to appear. From the 4th instar onwards, females typically took less time than males to reach each instar. From the 5th instar onwards, females were longer than the males, and were longer as adults. Variation in developmental pattern (number of instars) was evident among siblings from the same ootheca; such intra-clutch variability in number of instars may be a bet-hedging strategy by ovipositing females in a variable environment. The laboratory data allowed for the detection of six-instar and seven-instar patterns among the field-collected females. The field-collected data suggest that females undergoing 6 nymphal instars reach adulthood later in the season, and at smaller body size, than seven-instar females.

Introduction

Body size is an important feature of organisms, influencing many components of life history and fitness (Peters 1983; Roff 1992; Stearns 1992; Hone & Benton 2005). In many organisms, increased body size confers benefits, such as increased diet breadth, longevity, mating success and reproductive output, both between and within species (Wilson 1975; Peters 1983; Honěk 1993; Cohen et al. 1993; Andersson 1994; Bonduriansky 2001; Kingsolver & Pfenning 2004; Kingsolver & Huey 2008; Chown & Gaston 2010). These patterns are seen in insects, including orthopteroids, where large body size often correlates with longevity and reproductive success within species (Honěk 1993; Sokolovska et al. 2000; Akman & Whitman 2008; Whitman 2008). Yet, large body size can involve costs as well, such as increased metabolic, ecological, and movement costs (Peters 1983; Gotthard et al. 1994; Blanckenhorn 2000; Hone & Benton 2005; Teuschl et al.2007).

Body size is particularly important for solitary predators, whose food intake hinges on individual predation success, which, in turn, is often driven by the relative sizes of predator and prey (Wilson 1975; Claessen et al. 2002; McCoy et al. 2011). Praying mantids (Order Mantodea) are elongate solitary predators, whose body dimensions were predicted to influence prey size by Holling's morphometric models (Holling 1964; Holling et al. 1976). Indeed, natural mantid populations exhibit considerable intraspecific size variation, and this variation has ecological and reproductive consequences. In the field, length variation has been documented among mantid nymphs ofthe same instar (Hurd & Eisenberg 1989), as well as among adult females within and between years (Matsura et al. 1975; Eisenberg et al. 1981; Maxwell & Eitan 1998; Maxwell & Frinchaboy, in press). In Tenodera aridifolia Saussure, larger nymphal instars are more likely to attack larger prey, in addition to being more likely to attack smaller conspecific instars (Hurd 1988; Iwasaki 1991; Whitman & Vincent 2008). For T. angustipennis Saussure, Matsura et al. (1975) suggest a positive relationship between body length and ootheca (egg case) mass. For Pseudomantis albofimbriata Stål, Barry (2013) indicates that longer adult females are more attractive to males than shorter females. In Stagmomantis limbata Hahn, female pronotum length positively correlates with prey size in the field, as well as fecundity and ootheca mass (Maxwell & Frinchaboy, in press).

Within a species, variation in adult size can be generated through a combination of intrinsic and extrinsic factors that affect juvenile development (Stearns 1992; Arendt 1997; Nylin & Gotthard 1998; Day & Rowe 2002; Whitman 2008; Whitman & Ananthakrishnan 2009; González-Suárez et al. 2011). In arthropods, particularly important factors include immature growth and developmental rates, the number of nymphal instars, the duration of each instar, and genetic differences between the sexes and individuals (Higgins 1992, 2000; Higgins & Rankin 1996; Fagan & Odell 1996; Davidowitz et al. 2004; Whitman 2008; Blanckenhorn 2000; Chown & Gaston 2010; González-Suárez et al. 2011). In mantids, differences in food per capita among early instars affects body size and mass (Hurd & Eisenberg 1984; Matsura et al. 1984; Hurd & Rathet 1986; Paradise & Stamp 1991; Fagan & Hurd 1994; Dusse & Hurd 1997; Moran & Hurd 1997). Interestingly, developmental asynchrony and differences in the number of nymphal instars can occur among mantids reared under relatively constant, standardized conditions in the laboratory (Didlake 1926; Roberts 1937a, 1937b; Matsura et al. 1984; Iwasaki 1992), as in other insects (Esperk et al. 2007). In the studies on mantids, examinations of size differences between adults of different numbers of instars have been hampered by too few individuals reaching adulthood (Matsura et al. 1984; Iwasaki 1992).

While intraspecific variation in the number of nymphal instars has been demonstrated in the laboratory for at least five mantid species, including Stagmomantis limbata, two questions remain unanswered: 1) how do differences in instar number translate into size differences in the adult stage, and 2) does instar number vary in nature? The present study addresses these two questions in the mantid S. limbata. With regard to the first question, mantids were raised in captivity on standardized diets, to allow for the expression of different developmental patterns and resultant differences in adult size (pronotum length). These data on size and developmental patterns were then used to address the second question about instar number in the field.

The present study also examined the relationships among adult size, the timing of adult emergence, and the number of instars in the field. In S. limbata, new adult females can be readily identified by the diffuse yellow coloration of their underwings (Maxwell et al. 2010; Maxwell & Frinchaboy, in press). In nature, a negative correlation consistently appears between adult female pronotum length and the date of adult emergence (Maxwell & Frinchaboy, in press); that is, longer females emerge as adults earlier in the season, as appears to occur in other mantids (e.g., Prokop & Vaclav 2008). The present study sought to determine whether developmental patterns (i.e., number of instars) corresponded to date of adult emergence and adult length; that is, whether longer, early-maturing females typically underwent 6 or 7 nymphal instars.

Methods

Laboratory-reared, 1992.— To obtain mantids for rearing, nine oothecae were collected from field sites in Davis, California (3 8° 33′ N, 121 °44′W) in October 1991. The oothecae were kept in ventilated containers in a shaded outdoor shelter until 01 April 1992, when they were brought into an environmental chamber maintained at 25 °C. As part of an ecological study, the chamber's initial photoperiod was (12.5L:11.5D), and was changed 30 minutes every two weeks, to simulate the progress of the season, with one-month stases centered around midsummer and midwinter (15L:9D and 10L:14D, respectively). All developmental stages, from hatching through adulthood, were maintained in the environmental chamber.

The oothecae were checked daily for hatching. Hatching occurredbetween 29 April 1992 and 27 May 1992. The nine oothecae produced 915 hatchlings in total. Hatching is assigned as the start of the first nymphal instar. Hatchlings from the same ootheca that hatched on the same day were grouped into ventilated containers to track hatching date. The first three instars were group-reared (density = 1 nymph per 100 ml), and were misted daily with water. Each group of nymphs was checked daily for deaths and new molts. For the 1st and 2nd instars, each group was provided with abundant Drosophila melanogaster Meigen every two days. For the 3rd instar, each group was provided with abundant Drosophila virilis Sturtevant and house cricket hatchlings (Acheta domesticus L.) every two days. Upon reaching the 4th instar, each nymph was isolated in a 1.6-literventilated container and was fed 1–2 cricket nymphs every two days until adult emergence. Upon emerging as an adult, each mantid was fed to satiation with cricket nymphs and maintained in captivity until death.

Developmental data were recorded for the isolated mantids. Starting at the 4th instar, the date of each molt was recorded, allowing for instar duration to be calculated for instars 4–7. For instars 5–7 and adults, pronotum length was measured at each stage (to 0.1 mm). Forinstars 6–7 and adults, Dyar's coefficient at each stage was calculated as pronotum length (mm) at stage/pronotum length (mm) at the immediately preceding stage (Dyar 1890; Cole 1980). For adults, total developmental time (hatch-to-adult interval, in days) was calculated, as well as overall growth rate (pronotum length upon adult emergence/hatch-to-adult interval).

Field-collected females, 2011.—Late-instar female nymphs were collected via visual searching in field sites in Bishop and Big Pine, California (37°22′ N, 118°24′W and 37 ° 10′ N, 118° 17′ W, respectively) during 16′24 Aug 2011. At these sites, S. limbata is univoltine, with hatching occurring in May, adults first emerging in August, egg-laying occurring in Sept-Oct, and the oothecae overwintering.

Each nymph was isolated in a ventilated 1.6-liter container kept in a shaded outdoor shelter at the Owens Valley Laboratory (University of California property, Bishop, California). Each nymph was provided with misted water and one house cricket nymph every two days. The nymphs were checked daily for molting and adult emergence. Each nymph was measured for pronotum length (0.1 mm) upon capture and after each molt. These methods resulted in 50 adult females. Each adult was measured for pronotum length. Adult females were provided a standardized diet of one house cricket nymph every two days, and were maintained in captivity until death.

To assign developmental patterns to these field-collected females, I used pronotum length data from the females reared in 1992. Because the females in 1992 were of known developmental schedules, I used their lengths in their final instars as benchmarks to apply to the field-collected females. Females reared in the laboratory in 1992 underwent either six or seven nymphal instars before emerging as adults. For each of these developmental patterns, I calculated the mean pronotum length in the final nymphal instar, and constructed lsd and 2sd intervals around the mean (i.e., 1 and 2 standard deviations, respectively). I utilized overlap between the lsd and 2sd intervals to determine developmental patterns for the field-collected females, while minimizing the error of misassigning a given female's pattern.

Statistical analysis.—Statistical analyses were performed using SPSS 17.0 (IBM Co., Chicago, Illinois, USA). All inferential tests were two-tailed, and mean and standard error values were reported for descriptive statistics. Examination of developmental parameters (e.g., hatch date, instar duration, pronotum length at stage, Dyar's coefficient; Table 1) involved comparisons among females, and between males and females collectively. For these comparisons, I performed multiple univariate tests, thereby lowering alpha (a) according to the sequential Bonferroni technique (Rice 1989). Normality of these data was assessed by the Shapiro-Wilk test for normality; data with significant departures from normality (p < 0.05) were subject to transformation.

Results

Laboratory-reared.—Of the 915 hatchlings, 79 reached adulthood: 36 females and 43 males (Table 1). Of the 36 females, 23 reached adulthood aftersixinstars (“six-instarfemales”), while the remaining 13 reached adulthood after seven instars (“seven-instar females”). Of the 43 males, four reached adulthood after five instars (“fiveinstar males”), while the remaining 39 reached adulthood after six instars (“six-instar males”). The mean date of hatching was similar for the females and males, with the males tending to hatch two days earlier than the females (Table 1). Hatch date and two other developmental parameters (duration of 5th instar, duration of 6th instar) were found to significantly depart from normality. These data were subject to reciprocal-transformation (X′ = 1/X). Results for the statistical tests of transformed data are presented in Table 1; statistical significance did not differ between transformed and non-transformed data in any case.

Table 1.

Developmental parameters for laboratory-reared mantids (1992). Mean (SE) reported. Hatch-to-4th = number of days from hatching to emergence at 4th instar. Dyar's coefficient = pronotum length at stage (mm) / pronotum length at immediately preceding stage (mm). Hatch-to-adult = number of days from hatching to adult emergence. Growth rate = pronotum length at adult (mm) / hatch-to-adult (d).

t01_49.gif

Fig. 1.

Pronotum length at various stages for laboratoryreared females and males (1992). 5 = 5th instar; 6 = 6th instar; 7 = 7th instar; A = adult. White circles = seveninstar females; black circles = six-instar females; white diamonds = six-instar males; black diamonds = five-instar males.

f01_49.jpg

Males and females differed in development (Fig. 1, Table 1). Males took longer than females to reach the 4th instar, the durations of the 5th and 6th instars were longer for males than females, and average hatch-to-adult interval was four days longer for males than females. Yet, females and males had similar adult emergence dates: August 4 and August 6, respectively. The sexes differed in pronotum length and Dyar's coefficient (Fig. 1, Table 1). On average, females were longer than males at the 5th and 6th instars, as well as adulthood. Similarly, females exhibited higher Dyar's coefficients at 6th instar and adulthood.

Within-sex differences in development were evident for females (Fig. 1; Table 1). By the 4th instar, the seven-instar females already showed accelerated development, reaching this instar more quickly than the six-instar females. Seven-instar females completed the 4th, 5th, and 6th instars more quickly than six-instar females. Interestingly, the time to reach adulthood and the actual date of adult emergence did not significantly differ between the two groups of females. The shorter durations ofthe 4th and 5th instars forthe seveninstar females compromised their body size, as they were shorter than the six-instar females at the 5th and 6th instars (Table 1). The extra 7th instar, however, enabled the seven-instar females to attain larger adult size than the six-instar females (Table 1). Growth was similar between both groups of females throughout development, whether measured by Dyar's coefficient at 6th instar and adulthood or by overall growth rate to adulthood (Table 1).

Among females, the date of adult emergence was positively correlated with the date of hatching (Pearson correlation: r = 0.63, p < 0.001, all females combined). Differentiating females by developmental pattern did not change this positive relationship (Linear regression: adjusted r2 = 0.37, F233 = 11.42, whole-model p < 0.001; Date of hatching p < 0.001, Developmental pattern p > 0.4). Thus, females that hatched later in the calendar emerged as adults later, regardless of developmental pattern.

Comparison of developmental parameters is somewhat difficult among males, as the small number of five-instar males (n = 4) precludes statistical analysis. Despite the small sample size, these five-instar males showed shorter time to adulthood and shorter prontoum length than the six-instar males (Fig. 1, Table 1). For all males combined, the date of adult emergence was positively correlated with the date of hatching (Pearson correlation: r = 0.62, p < 0.001). This relationship persisted when only examining six-instar males (Pearson correlation: r = 0.67, p < 0.001).

Regarding adult pronotum length and the calendar date of adult emergence, no correlation was evident for all females combined (Fig. 2a; Pearson correlation: r = -0.17, p > 0.3). Differentiating females by developmental pattern revealed a negative relationship between adult pronotum length and adult emergence date (Linear regression: adjusted r2 = 0.53, F2,32 = 20.01, whole-model p < 0.001; Date of emergence p = 0.032, Developmental pattern p < 0.001), with the regression coefficient for Date of emergence = -0.06 (SE = 0.03). For all males combined, adult pronotum length did not correlate with emergence date (Fig. 2a; Pearson correlation: r = 0.08, p > 0.5); restricting analysis to six-instar males did not change this result (Pearson correlation: r = -0.16, p > 0.3).

As the hatching period spanned one month (29 April to 27 May), hatching date can be standardized for all adults by examining the total developmental period (hatch-to-adult, in days). For all females combined, a negative correlation was detected between developmental period and adult pronotum length (Fig. 2b; Pearson corrleation: r = -0.37, p < 0.05). This negative relationship persisted when differentiating females by developmental pattern (Linear regression: adjusted r2 = 0.68, F2,32 = 37.73, whole-model p < 0.001; Developmental period p < 0.001, Developmental pattern p < 0.001), with the regression coefficient for Developmental period = -0.12 (SE = 0.03). For all males combined, developmental period did not correlate with pronotum length (Fig. 2b; Pearson correlation: r = -0.24, p > 0.1). Examination of six-instar males, however, showed a negative relationship (Pearson correlation: r = -0.63, p < 0.001 ), as the shorter five-instar males tended to develop more quickly, thereby weakening the overall negative relationship.

Fig. 2.

Adult pronotum length vs time for laboratory-reared females and males (1992). White circles = seven-instar females; black circles = six-instar females; white diamonds = six-instar males; black diamonds = five-instar males, a) Calendar date of adult emergence, b) Developmental period (hatch-to-adult), in days.

f02_49.jpg

Variation in development was evident within sibling groups (i.e., within a single ootheca). With regard to females, six of the nine oothecae produced both six-instar and seven-instar adults. Three such oothecae are illustrated in Fig. 3, each producing 6–8 adult females in total. Within each ootheca, the females typically hatched on the same calendar day, but showed considerable variation in pronotum length at adulthood, hatch-to-adult interval, and hatch-to-adult growth rates (indicated by individual lines in Fig. 3). Variation in growth rates (slope of lines) was evident for females of the same developmental schedule within an ootheca (e.g., seveninstar females in Fig. 3a, and six-instar females in Fig. 3b). With regard to males, the 4 five-instar adults emerged from the same ootheca; this ootheca produced 6 six-instar males as well.

Final-instar pronotum lengths for the laboratory-reared females showed separation between six-instar and seven-instar females, with some overlap in the range 15.2–16.5 mm (Fig. 4a). The 1sd and 2sd intervals for six-instar and seven-instar females are indicated in Fig. 4a. While 1sd intervals for six-instar and seven-instar females do not overlap, using these intervals as the bases for assigning developmental schedules to field-collected females risks assignment error. For example, two seven-instar females from the laboratory lay within the 1sd interval for six-instar females (i.e., seven-instar females of final-instar lengths 15.2 and 15.4 mm in Fig. 4a). Using the non-overlapping regions within the 2sd intervals largely avoids misassignment, as follows. With regard to the six-instar females from the laboratory, the region of the 2sd interval that does not overlap with the seven-instar 2sd interval is 13.3–14.7; this region only includes six-instar females. Similarly, the non-overlapping region ofthe 2sd interval for seven-instar females is 16.2–19.2 mm (Fig. 4a). All but one of the females in this region are seven-instar females; the lone six-instar female lies at the minimum value of this range (16.2 mm).

Fig. 3.

Variation in developmental pattern among females within oothecae (1992). Each panel (a, b, c) is a different ootheca. Lines indicate growth rates for individual females. Data points on the x-axis represent the date of hatching (pronotum length at hatching is set to 0.0 mm). Data points above the x-axis depict the date of adult emergence and corresponding adult pronotum length. White circles and solid lines = seven-instar females; black circles and dashed lines = six-instar females.

f03_49.jpg

Fig. 4.

Female pronotum length, a) Laboratory-reared (1992). x-axis = pronotum length at final nymphal instar. Black circles = six-instar females; white circles = seven-instar females. At bottom of panel are shown mean final instar pronotum length for six-instar females (black) and seven-instar females (white), with ±1 standard deviation (vertical tick marks) and ±2 standard deviations (ends of horizontal lines) shown for each mean, b) Field-collected (2011). x-axis = pronotum length at final nymphal instar. Black circles = females assigned to six-instar pattern; gray circles = females assigned to seven-instar pattern; white triangles = females not assigned to developmental pattern. As reference for the criteria for assigning females to developmental patterns, at bottom of panel are shown mean final instar pronotum lengths for six-instar females (black) and seven-instar females (white) from 1992, with ±1 standard deviation and ±2 standard deviations shown for each mean, c) Field-collected (2011). x-axis = date of adult emergence. Black circles = females assigned to sixinstar pattern; gray circles = females assigned to seven-instar pattern; white triangles = females not assigned to developmental pattern.

f04_49.jpg

Field-collected females.—Forthe field-collected female nymphs, finalinstar pronotum lengths spanned 14.0–18.5 mm (n = 50; Fig. 4b). This range was contained within the 2sd intervals of the six-instar and seven-instar females from the laboratory (indicated in Fig. 4b). Applying the criterion of non-overlapping 2sd intervals to the field-collected nymphs, distinguishablesix-instarfemales(14.7 mm or less in pronotum length, n = 9) and seven-instar females (16.2 mm or greater in pronotum length, n = 17) were revealed, with the remaining females not being assigned to developmental patterns (Fig. 4b). A negative relationship was observed between date of adult emergence and adult pronotum length for the field-collected females (Pearson correlation: r = -0.39, p < 0.01, n = 50; Fig. 4c).

Seven-instar females emerged as adults within the period 22 Aug - 06 Sep (mean ± SE = Aug 28 ± 1, n = 17). While a substantial proportion of six-instar females also emerged as adults within this period (67%), a number of particularly late-emerging six-instar females resulted in the mean date of emergence being significantly later than seven-instar females (six-instar mean ± SE date of emergence = Sep 6 ± 4, n = 9; t-test: t24 = 3.2, p < 0.01).

For all field-collected females combined, mean ± SE Dyar's coefficient = 1.31 + 0.01 (n = 50). This value was very similar to the overall mean forthe 1992 laboratory-reared females (mean ± SE = 1.32 ± 0.01; Table 1). For the field-collected females, Dyar's coefficient at adulthood did not significantly differ between six-instar females (1.32 ± 0.01, n = 9) and seven-instar females (1.30 ± 0.01, n = 17; t24 = 1.68, p > 0.1).

Discussion

The present study answers several questions regarding developmental patterns and body size in Stagmomantis limbata. For the laboratory-reared mantids (1992), females showed the most variation in developmental pattern. The majority of females underwent a six-instar pattern to adulthood (64%), with the remaining 36% following a seven-instar pattern. Differences between these two patterns were evident by the 4th instar. Seven-instar females showed an accelerated developmental pace, reaching the 4th instar more quickly than six-instar females, as well as shortening the durations of the 4th, 5th, and 6th instars. This quickened pace allowed for the additional 7th instar to be completed without substantially delaying the total time taken to reach adulthood, as the developmental period from hatching to adult emergence did not significantly differ between seven-instar and six-instar females. The shorter times taken to reach the 4th, 5th, and 6th instars in the laboratory compromised body size forthe seven-instar females, as these females were shorter than six-instar females at the 5th and 6th instars. The additional 7th instar, however, resulted in seven-instar females being significantly longerthan six-instar females at adulthood. Growth rate was similar between seven-instar and six-instar females, whether measured as Dyar's coefficient or as overall growth rate to adulthood.

Most ofthe lab-reared males followed a six-instar pattern (91%), with the remaining 9% following a five-instar pattern. Six-instar males required more days to reach adulthood than five-instar males, and emerged as longer adults. In the laboratory, clear and persistent differences were evident between the sexes by the 4th and 5th instars. From the 4th instar onwards, females typically took less time to reach each instar. From the 5th instar onwards, females were longer than the males, and showed higher Dyar's coefficients at the 6th instar and adulthood. In many species within the Mantodea, females are longer than males (Roy 1999; Ehrmann 2002). The present study contributes towards an understanding of the ontogeny of this sexual size dimorphism, as developmental differences between the sexes were obvious by the 4th and 5th instars. How much earlier in development that these differences can be detected remains unknown for S. limbata. In the mantid P. albofimbriata, Allen et al. (in press) indicate that males and females significantly differ in size as early as the second instar. The onset of sexual size dimorphism warrants further investigation, as this question is unresolved for many invertebrates (Abbott & Svensson 2008; Stillwell et al. 2010).

This study identified both six- and seven-instar patterns in females in the field, thereby demonstrating developmental variation in nature. The field results also suggested that six-instar females emerge as adults later than seven-instar females. These results tend to support the hypothesis that early-emerging adults undergo more molts in nature, albeit with some caveats. For the field-collected females, there was substantial overlap between the adult emergence dates of six-instar and seven-instar females. Yet, a small number of particularly late-emerging six-instar females resulted in the mean dates of emergence differing. This could be a statistical artifact, especially considering that, in the laboratory, the total developmental period (hatch-to-adult) and calendar date of adult emergence did not differ significantly between six-instar and seven-instar females. Furthermore, previous studies on S. limbata and other mantids did not report differences in the durations of developmental patterns for females (Roberts 1937a, 1937b; Matsura et al. 1984), and Iwasaki (1992) actually indicated longer developmental periods for seveninstar males than for six-instar males in T. aridifolia. Clearly, these conflicting results call for more research on this question.

One critique of the present study is that laboratory developmental patterns derived from a population of S. limbata from Davis, CA in 1992 may not apply to field-collected S. limbata from Bishop, CA in 2011. Examination of the final instar lengths of the field-collected females, however, clearly reveals the assigned six-instars as a distinct, separate cluster of the smallest individuals (i.e., lower left cluster in Fig. 4b). It seems reasonable to conclude that these individuals are indeed six-instar females, even without reference to the laboratory data, thus allowing for a comparison of adult-emergence of six- vs seven-instar females in the field. Furthermore, the overall mean Dyar's coefficients at adulthood for the laboratory-reared and fieldcollected females are nearly identical (1.32 and 1.31, respectively), suggesting consistent underlying developmental physiology.

The field and laboratory data generally corroborate the negative relationship between adult female pronotum length and date of adult emergence, as documented in nature for S. limbata (Maxwell & Frinchaboy, in press). For the laboratory-reared females, however, this negative relationship was somewhat weak when pronotum length was examined against calendar date of adult emergence. A weak relationship may be attributable to variation in hatch dates, as later-hatching seven-instar females may push large pronotum length values towards later dates (Fig. 2a). This effect was evident in the present study. When hatching date was standardized by examining the developmental period (hatch-to-adult interval), a stronger negative correlation was found between pronotum length and developmental period (Fig. 2b). Thus, when adults are confined to a standardized hatching date, a stronger negative relationship between pronotum length and time becomes evident. In nature, therefore, the consistent negative relationship between adult female pronotum length and adult emergence date in S. limbata might be a reflection of the following factors: a narrow window for hatching and, for a given developmental pattern, slowly-growing individuals emerging as adults later and smaller. A critical time in the season, by which immatures must mature in order to reproduce, might compel slow-growers to emerge at particularly small sizes, thereby generating a even stronger negative relationship between adult length and emergence date (Higgins & Rankin 1996; Higgins 2000; Maxwell & Frinchaboy, in press).

The present study raises the question of why variation in instar number exists in this species. Proximate explanations of this variation point to various environmental and genetic influences (Higgins & Rankin 1996; Esperk et al. 2007; González-Suárez et al. 2011; Chown & Gaston 2010). One such environmental influence is food availability during development (Esperk et al. 2007). Food availability, however, does not seem to account for the occurrence of early-emerging adult six-instar females, both in the laboratory and collected from the field. That is, such females, isolated and regularly supplied with prey, might be expected to continue feeding to undergo a 7th instar to emerge at larger adult size. Other environmental influences on the number of instars include the date of hatching and microhabitat temperature (Higgins 2000; Esperk et al. 2007; Chown & Gaston 2010; Dmitriew 2010). Neither hatching date nor temperature, however, appears to explain the present study's variation within oothecae, where laboratory-reared females that hatched on the same day and reared under the same temperature followed different developmental patterns (Fig. 3). Other factors, such as genetic or maternally-induced differences between individuals, remain possible explanations of this study's different developmental patterns.

A separate question is the adaptive value of the different developmental patterns (Stearns 1992; Arendt 1997; Nylin & Gotthard 1998; Whitman & Agrawal 2009). In S. limbata, an individual&s number of instars might be a particular developmental strategy, especially if different developmental patterns entail separate costs and benefits. While seven-instar females are typically longer and are therefore expected to reap benefits such as increased fecundity (Maxwell & Frinchaboy, in press), large size most likely includes nutritional and energetic costs (Peters 1983; Blanckenhorn 2000). Furthermore, each molt involves risks to the individual, including deformities due to molting errors and vulnerability to predators (personal observations; see Whitman 2008), which potentially add costs to the seven-instar pattern. Thus, each developmental pattern might be viable, as each represents an evolutionary solution to the challenges of survival and reproduction.

Further research on environmental and genetic effects will shed light on the factors that determine the developmental pattern of a given individual. The possibility of genetically- or maternally-determined developmental patterns, together with observations of different developmental patterns among sibling females, suggests the intriguing notion of bet-hedging by egg-laying females; that is, producing variation in developmental patterns among progeny within a brood. Such an integration of the proximate factors that determine developmental pattern with considerations of the fitness consequences of body size will provide much insight into the evolution of life histories.

Acknowledgments

I thank Gilbert Amparo, Danielle Bruno, Robyn lacobi, and Thanh Maxwell for assistance with rearing and maintaining mantids. Comments by reviewers improved this paper. I additionally thank the staff of the Owens Valley Laboratory (University of California, White Mountain Research Station) for accommodations and logistical support. National University and the University of California at Davis provided funding for this research.

References

1.

J.K. Abbott , E.I. Svensson 2008. Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs. Evolutionary Ecology 22: 103–21. Google Scholar

2.

O. Akman , D.W. Whitman 2008. Analysis of body size and fecundity in a grasshopper. Journal of Orthoptera Research 17: 249–257. Google Scholar

3.

L.E. Allen , K.L. Barry , G.I. Holwell In press. Different paths to sexual size dimorphism in two praying mantids, Pseudomantis albofimbriata and Hierodula majuscula. Insect Science. Google Scholar

4.

M. Andersson 1994. Sexual Selection. Princeton University Press, Princeton, New Jersey. Google Scholar

5.

J.D. Arendt 1997. Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 72: 149–177. Google Scholar

6.

K.L. Barry 2013. You are what you eat: food limitation affects reproductive fitness in a sexually cannibalistic praying mantid. PLoS One 8: e78164. Google Scholar

7.

W.U. Blanckenhorn 2000. The evolution of body size: what keeps organisms small? Quarterly Review of Biology 75: 385–407. Google Scholar

8.

R. Bonduriansky 2001. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews 76: 305–339.  Google Scholar

9.

S.L. Chown , K.J. Gaston 2010. Body size variation in insects: a macroecological perspective. Biological Reviews 85: 139–169. Google Scholar

10.

D. Claessen , C. van Oss , A.M. de Roos , L. Persson 2002. The impact of size-dependent predation on population dynamics and individual life history. Ecology 83: 1660–1675. Google Scholar

11.

J.E. Cohen , S.L. Pimm , P. Yodzis , J. Saldaña 1993. Body sizes of animal predators and animal prey in food webs. Journal of Animal Ecology 62: 67–78. Google Scholar

12.

B.J. Cole 1980. Growth ratios in holometabolous and hemimetabolous insects. Annals of the Entomological Society of America 73: 489–491.  Google Scholar

13.

G. Davidowitz , L.J. D'Amico , H.F. Nijhout 2004. The effects of environmental variation on a mechanism that controls insect body size. Evolutionary Ecology Research 6: 49–62. Google Scholar

14.

T. Day , L. Rowe 2002. Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. American Naturalist 159: 338–350. Google Scholar

15.

M. Didlake 1926. Observations on the life-histories of two species of praying mantis (Orthopt.: Mantidae). Entomological News 37: 169–174.  Google Scholar

16.

C.M. Dmitriew 2010. The evolution of growth trajectories: what limits growth rate? Biological Reviews 86: 97–116. Google Scholar

17.

K. Dusse , L.E. Hurd 1997. Food limitation reduces body length in mantid nymphs, Tenodera sinensis Saussure (Mantodea: Mantidae): implications for fitness. Proceedings of the Entomological Society of Washington 99: 490–493. Google Scholar

18.

H.G. Dyar 1890. The number of molts of lepidopterous larvae. Psyche 5: 420–422. Google Scholar

19.

R. Ehrmann 2002. Mantodea: Gottesanbeterinnen der Welt. Natur undTier, Münster, Germany. Google Scholar

20.

R.M. Eisenberg , L.E. Hurd , J.A. Bartley 1981. Ecological consequences of food limitation for adult mantids (Tenodera aridifolia sinensis Saussure). American Midland Naturalist 106: 209–218. Google Scholar

21.

T. Esperk , T. Tammaru , S. Nylin 2007. Intraspecific variability in number of larval instars in insects. Journal of Economic Entomology 100: 627–645. Google Scholar

22.

W.F. Fagan , L.E. Hurd 1994. Hatch density variation of a generalist arthropod predator: population consequences and community impact. Ecology 75: 2022–2032. Google Scholar

23.

W.F. Fagan , G.M. Odell 1996. Size-dependent cannibalism in praying mantids: using biomass flux to model size-structured populations. American Naturalist 147: 230–268. Google Scholar

24.

M. González-Suárez , J.F. Le Galliard , D. Claessen 2011. Population and lifehistory consequences of within-cohort individual variation. American Naturalist 178: 525–537. Google Scholar

25.

K. Gotthard , S. Nylin , C. Wiklund 1994. Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99: 281–289. Google Scholar

26.

L.E. Higgins 1992. Developmental plasticity and fecundity in the orb-weaving spider Nephila clavipes. Journal of Arachnology 20: 94–06. Google Scholar

27.

L.E. Higgins 2000. The interaction of season length and development time alters size at maturity. Oecologia 122: 51–59. Google Scholar

28.

L.E. Higgins , M.A. Rankin 1996. Different pathways in arthropod postembryonic development. Evolution 50: 573–582. Google Scholar

29.

C.S. Holling 1964. The analysis of complex population processes. Canadian Entomologist 96: 335–347. Google Scholar

30.

C.S. Holling , R.L. Dunbrack , L.M. Dill 1976. Predator size and prey size: presumed relationship in the mantid Hierodula coarctata Saussure. Canadian Journal of Zoology 54: 1760–1764. Google Scholar

31.

D.W.E. Hone , M.J. Benton 2005. The evolution of large size: how does Cope's Rule work? Trends in Ecology and Evolution 20: 4–6. Google Scholar

32.

A. Honěk 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66: 483–492. Google Scholar

33.

L.E. Hurd 1988. Consequences of divergent egg phenology to predation and coexistence in two sympatric, congeneric mantids (Orthoptera: Mantidae). Oecologia 76: 549–552. Google Scholar

34.

L.E. Hurd , R.M. Eisenberg 1984. Experimental density manipulations of the predator Tenodera sinensis (Orthoptera: Mantidae) in an old-field community. I. Mortality, developmental and dispersal of juvenile mantids. Journal of Animal Ecology 53: 269–281. Google Scholar

35.

L.E. Hurd , R.M. Eisenberg 1989a. A mid-summer comparison of sizes and growth rate. Proceedings of the Entomological Society of Washington 91: 51–54. Google Scholar

36.

L.E. Hurd , I.H. Rathet 1986. Functional response and success in juvenile mantids. Ecology 67: 163–167. Google Scholar

37.

T. Iwasaki 1991. Predatory behavior of the praying mantis, Tenodera aridifolia. II. Combined effect of prey size and predator size on the prey recognition. Journal of Ethology 9: 77–81. Google Scholar

38.

T. Iwasaki 1992. Stage duration, size and coloration of two praying mantises, Tenodera aridifolia (Stoll) and Tenodera angustipennis Saussure (Mantodea, Mantidae). Japanese Journal of Entomology 60: 551–557. Google Scholar

39.

J.G. Kingsolver , R.B. Huey 2008. Size, temperature, and fitness: three rules. Evolutionary Ecology Research 10: 251–268. Google Scholar

40.

J.G. Kingsolver , D.W. Pfennig 2004. Individual-level selection as a cause of Cope's Rule of phyletic size increase. Evolution 58: 1608–1612. Google Scholar

41.

T. Matsura , T. Inoue , Y. Hosomi 1975. Ecological studies of a mantid, Paratenodera angustipennis de Saussure. I. Evaluation of the feeding condition in natural habitats. Researches Population Ecology 17: 64–76. Google Scholar

42.

T. Matsura , H. Yoshimaya , T. Nagai 1984. Growth, prey consumption and food assimilation efficiency in a mantid, Paratenodera angustipennis (S.). Kontyu (Tokyo) 52: 37–49. Google Scholar

43.

M.R. Maxwell , O. Eitan 1998. Range expansion of an introduced mantid Iris oratoria and niche overlap with a native mantid Stagmomantis limbata (Mantodea: Mantidae). Annals of the Entomological Society of America 91: 422–429. Google Scholar

44.

M.R. Maxwell , C. Frinchaboy In press. Consequences of intraspecific variation in female body size in the mantid Stagmomantis limbata (Mantodea: Mantidae): feeding ecology, male attraction, and egg production. Environmental Entomology. Google Scholar

45.

M.R. Maxwell , K.M. Gallego , K.L. Barry 2010. Effects offemale feeding regime in a sexually cannibalistic mantid: fecundity, cannibalism, and male response in Stagmomantis limbata (Mantodea). Ecological Entomology 35: 775–787. Google Scholar

46.

M.W. McCoy , B.M. Bolker , K.M. Warkentin , J.R. Vonesh 2011. Predicting predation through prey ontogeny using size-dependent functional response models. American Naturalist 177: 752–766. Google Scholar

47.

M.D. Moran , L.E. Hurd 1997. Relieving food limitation reduces survivorship of a generalist predator. Ecology 78: 1266–1270. Google Scholar

48.

S. Nylin , K. Gotthard 1998. Plasticity in life-history traits. Annual Review of Entomology 43: 63–83. Google Scholar

49.

C. J. Paradise , N.E. Stamp 1991. Abundant prey can alleviate previous adverse effects on growth of juvenile praying mantids (Orthoptera: Mantidae). Annals of the Entomological Society of America 84: 396–406. Google Scholar

50.

R.H. Peters 1983. The Ecological Implications of Body Size. Cambridge University Press, Cambridge, UK. Google Scholar

51.

P. Prokop , R. Vaclav 2008. Seasonal aspects of sexual cannibalism in the praying mantis (Mantis religiosa). Journal of Ethology 26: 213–218. Google Scholar

52.

W.R. Rice 1989. Analyzing tables of statistical tests. Evolution 43: 223–225. Google Scholar

53.

R.A. Roberts 1937a. Biology of the bordered mantid, Stagmomantis limbata Hahn (Orthoptera, Mantidae). Annals of the Entomological Society of America 30: 96–109. Google Scholar

54.

R.A. Roberts 1937b. Biology of the minor mantid, Litaneutria minor Scudder (Orthoptera, Mantidae). Annals of the Entomological Society of America 30: 111–119. Google Scholar

55.

D.A. Roff 1992. The Evolution of Life Histories. Chapman and Hall, New York. Google Scholar

56.

R. Roy 1999. Morphology and taxonomy, pp. 19–40. In: F.R. Prete , H. Wells , P.H. Wells , L.E. Hurd (Eds), The Praying Mantids. Johns Hopkins University Press, Baltimore, Maryland. Google Scholar

57.

N. Sokolovska , L. Rowe , F. Johansson 2000. Fitness and body size in mature odonates. Ecological Entomology 25: 239–248. Google Scholar

58.

S.C. Stearns 1992. The Evolution of Life Histories. Oxford University Press, Oxford, UK. Google Scholar

59.

R.C. Stillwell , W.U. Blanckenhorn , T. Teder , G. Davidowitz , C.W. Fox 2010. Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annual Review of Entomology 55: 227–245. Google Scholar

60.

Y. Teuschl , C. Reim , W.U. Blanckenhorn 2007. Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies. Journal of Evolutionary Biology 20: 87–103. Google Scholar

61.

D.W. Whitman 2008. The significance of body size in the Orthoptera: a review. Journal of Orthoptera Research 17: 117–134. Google Scholar

62.

D.W. Whitman , A.A. Agrawal 2009. What is phenotypic plasticity and why is it important? pp. 1–63. In: D.W. Whitman , T.N. Ananthakrishnan (Eds) Phenotypic Plasticity of Insects: Mechanisms and Consequences. Science Publishers, Enfield, New Hampshire. Google Scholar

63.

D.W. Whitman , T.N. Ananthakrishnan (Eds) 2009. Phenotypic Plasticity of Insects: Mechanisms and Consequences. Science Publishers, Enfield, New Hampshire. Google Scholar

64.

D.W. Whitman , S. Vincent 2008. Large size as an antipredator defense in an insect. Journal of Orthoptera Research 17: 353–371. Google Scholar

65.

D.S. Wilson 1975. The adequacy of body size as a niche difference. American Naturalist 109: 769–784. Google Scholar
Michael R. Maxwell "Developmental Patterns in Stagmomantis limbata (Mantodea: Mantidae): Variation in Instar Number, Growth, and Body Size," Journal of Orthoptera Research 23(1), 49-58, (1 July 2014). https://doi.org/10.1665/034.023.0104
Published: 1 July 2014
JOURNAL ARTICLE
10 PAGES


SHARE
ARTICLE IMPACT
Back to Top