Life history and nesting ecology of a Japanese tube-nesting spider wasp Dipogon sperconsus (Hymenoptera: Pompilidae)

Nesting records

Dipogon nests were created singly per cane, because there were no examples in which wasps of two species emerged from the same cane in the study site. Thus, we designate “utilized canes” as “nests”.

In the four years, in pine forests in Takarazuka, Hyogo, Japan, we collected a total of 419 nests with 1033 cells from which species of Dipogon emerged (Fig. 1; Table 1; Supplementary Table S1). The numbers of nests and cells and the average and SD of the number of cells per nest for each species are shown in Table 1. Other wasps, bees, and parasitic wasps and flies also emerged from our trap nests (Supplementary Table S2), but we did not consider their nesting in the following analyses. Among 1033 cells, D. sperconsus emerged from 623 cells, D. inconspersus from 26 cells, and D. bifasciatus (Geoffroy) from 4 cells, while rearing failure occurred in 380 cells (Table 1), the owners of which we designate as “unknown Dipogon spp.” Based on the total cells of Dipogon, the proportion of cells constructed by D. sperconsus was 60.3% (623/1033*100), that of D. inconspersus was 2.5% (26/1033*100), and that of D. bifasciatus was 0.39% (4/1033*100). Based on the cells of the identified species, the proportion of cells constructed by D. sperconsus was 95.4% (623/(623 + 26 + 4)*100), that of D. inconspersus was 4.0% (26/(623 + 26 + 4)*100), and that of D. bifasciatus was 0.6% (4/(623 + 26 + 4)*100). From these proportions, we can estimate the number of cells constructed by the three species of Dipogon in the total 1033 Dipogon cells as ca. 985.5 cells (1033*0.954) by D. sperconsus, ca. 41.3 cells (1033*0.04) by D inconspersus, and ca. 6.2 cells (1033*0.006) by D. bifasciatus.

Because multiple cells were often constructed in a single nest, the number of nests was much smaller than the number of constructed cells. Among the 419 nests, 221 nests belonged to D. sperconsus, 7 nests belonged to D. inconspersus, and a single nest belonged to D. bifasciatus, but the remaining 190 nests could not be identified because of rearing failure (Table 1). The proportions of the nests in the three Dipogon species were calculated as follows: 96.5% (221/(221 + 7 + 1)*100) in D. sperconsus, 3.1% (7/(221 + 7 + 1)*100) in D inconspersus, and 0.4% (1/(221 + 7 + 1)*100) in D. bifasciatus. Thus, the estimated number of nests in each species was ca. 404.3 (419*0.965) in D. sperconsus, ca. 13.0 (419*0.031) in D inconspersus, and ca. 1.7 (419*0.004) in D. bifasciatus.

Next, we considered whether the cane bundles were used randomly. Based on the yearly frequency distributions of nests (Supplementary Tables S3–S6), we developed a null hypothesis assuming the nests are randomly distributed over bundles, where a negative binomial distribution is expected (Supplementary Tables S7–S8). Our yearly data indicate that the null hypothesis was rejected and that nests were more or less aggregated in a few bundles (Supplementary Figure S1; test statistics, Supplementary Table S8). This aggregation tendency (e.g., no nests in some bundles) may imply that some selected sites for bundles are not appropriate for D. sperconsus, for some unknown behavioral reasons. Further studies are needed to verify the habitat use of this species.

Yearly frequency distributions of the number of cells show that the range of cells constructed by D. sperconsus and unknown D. spp. combined were 1–10 cells, and the median was 2 cells (Supplementary Table S3–S6, Supplementary Figure S2). Most of the nests included 1–3 cells, and five or more cells were very rare. Most of the nests with many cells (e.g., 7–10 cells) were likely to be constructed by a single wasp because these wasps avoid interactions with other spider wasps. The average number of D. sperconsus cells per nest was 2.82 for four years, varying from 2.21 (2014) to 3.16 (2016) (Table 1), and the yearly differences were significant (Kruskal–Wallis test, (chi ^{2} = 7.70), df = 3, p = 0.05). In contrast, the average number of cells per nest of D. sayi sayi was slightly greater than that of D. sperconsus: 3.2 (1–6, SD = 1.47, n = 41) in the first generation and 4.7 (1–13, SD = 2.52, n = 107) in the second generation in Wisconsin, USA⁸; and 6.2 (1961), 4.0 (1962) and 3.0 (1963) in the summer generation and 7.5 (1961) and 3.2 (1962) in the overwintering generation in Northwestern Ontario⁹.

Life history of Dipogon sperconsus

Developmental period

The developmental period of reared wasps was estimated in the summer and overwintering generations separately (Table 2, Supplementary Figure S3, Supplementary Tables S9–S12). In the summer generation, both females and males developed from egg to adult over approximately three weeks (23.1 days for females and 21.6 days for males; Table 2). There was no significant difference between sexes (t-test, after adjustment by Bonferroni method: p > 0.05). In the overwintering generation, approximately eight months were required from egg to adult (246 days for females and 247 days for males). There was also no significant difference between sexes (t-test, after adjustment by Bonferroni method: p > 0.05). In females, all developmental periods were significantly longer in the overwintering generation than in the summer generation (t-test, after adjustment by Bonferroni method: p < 0.05). In males, a similar tendency was found, but there were significant differences between the two generations only in the prepupal and pupal periods (t-test, after adjustment by the Bonferroni method: p > 0.05 for egg and larval periods; p < 0.05 for prepupal and pupal periods).

The lengths of every developmental period of this species in the summer generation were almost the same as those of D. sayi sayi and D. papago anomalus in the summer generation (D. sayi sayi: egg period, 2 days; larval period, 5–6 days; prepupal and pupal periods, 14 days in Wisconsin, USA⁸; and egg period, 2 days; larval period, 5–7 days; prepupal and pupal periods, 13–16 days in males and 13–17 days in females in Plummers Island, Maryland, USA²; D. papago anomalus: egg period, 2 days; larval period, 5 days; prepupal and pupal periods, 18 days in Plummers Island².

Life cycle and voltinism

To examine the seasonal changes in nesting activities, we illustrated the developmental periods of individual wasps (Fig. 2) and the number of emerging wasps and the egg production for every 10 days of each month (Fig. 3). The egg production was calculated from the oviposition days estimated from the developmental stages and rearing data for individuals in nests collected over four years (Supplementary Tables S9–S12). Oviposition of D. sperconsus and unknown D. spp. began from mid-June to early July and continued until mid-September to early October (Supplementary Figure S3). Because the developmental period from egg to adult emergence is about 21–23 days for the summer generations (Table 2, Supplementary Tables S9–S12), it is theoretically possible that at most four or five generations emerge into adults over the whole nesting season (96 days in 2013, 88 days in 2014, 110 days in 2015 and 103 days in 2016; Supplementary Tables S9–S12). However, the actual number of generations per year appeared to be smaller: three in 2013 and 2015, and two or three in 2014 and 2016 (Figs. 2, 3a, Supplementary Figure S3). This discrepancy between the expected and observed number of generations could be explained by the fact that most of the eggs laid after early August became the overwintering generation (Fig. 2). We here call those eggs, the ‘overwintering’ eggs. The ‘overwintering’ eggs started appearing at the beginning of August (possibly late July, but no records) and sharply increased to become 100% early August (Fig. 3b).

The 50% ‘overwintering’ egg days were August 3 in 2013, August 6 in 2014, August 7 in 2015, and August 1 in 2016. These switching day varied about a week, but all fell in early August. Because there were only about 50 days available for nesting females from mid-June (earliest nesting activity) to early August (switching day), up to two generations could emerge before producing the overwintering generation. Thus, the present population has a life history with two or three generations per year, depending on how many generations emerge into adults before early August. Comparing the switching day (August 3 in 2013, August 6 in 2014, August 7 in 2015, August 1 in 2016) with the egg production peak in four years, the switching day was found to be around the second peak of oviposition in 2013, between the first and second peaks in 2014, and after the second peak (before the third peak) in 2015 (Fig. 3b). The switching day appeared to be immediately after the first peak in 2016 (Fig. 3b). However, if we regard a small rise in the cumulative number of eggs in the late June of 2016 as the first peak (Supplementary Figure S3), the switching day is immediately after the second peak in the year. These results indicate that in 2013, 2015 and 2016, the second generation mostly produced eggs for the third generation and a few eggs for the overwintering generation (i.e., most individuals are trivoltine), while in 2014 the second generation produced many eggs for the overwintering generation (i.e., most individuals are bivoltine).

The life cycle of this species typically seemed to proceed as follows: Wasps of both sexes in the overwintering (first) generation emerged almost simultaneously for approximately 10 days from late April to mid-May. The first-generation wasps laid eggs from mid-June to mid-July. There is about a two-month blank between emergence and oviposition in these ‘overwintering’ wasps. Hatched individuals of the eggs emerged from early July to early August (second generation). The offspring of the second generation had two possibilities. (1) Emerging in that summer becoming the third generation (when the second-generation females laid eggs before early August, these eggs became adults around mid- and late August), all the offspring of which entered into the overwintering stage (i.e., trivoltine). (2) Overwintering and emerging in the following year (when the second-generation females laid eggs in or after early August, these eggs became hibernating prepupae) (i.e., bivoltine). Thus, the voltinism of this species in the study site is variable between bivoltine and trivoltine, depending on the proportion of the eggs laid before early August by the second-generation females. We, however, could not exclude the possibility that a few early-developing individuals of the third generation emerged into adults before early August and that the fourth-generation adults appeared within a year (i.e., multivoltine). In summary, this species is plurivoltine. Similar plurivoltine was reported in D. sayi sayi. This wasp is bivoltine in Ontario⁹ and New York, USA², and probably trivoltine in Washington, D.C., USA².

There was a tendency for males in the overwintering generation to emerge earlier than females, but such a tendency was not noticeably demonstrated in the subsequent generations (Fig. 3a, Supplementary Table S13). The overall sex ratio was 0.43, slightly biased toward females. In D. sayi sayi, the sex ratios were 0.73 (1961), 0.5 (1962) and 0.38 (1963) in the summer generation and 0.38 (1961) and 0.5 (1962) in the overwintering generation in Northwestern Ontario⁹; 0.78 (35:10) in Washington County, USA¹⁶; and 0.29 (31:76) in Plummers Island².

To elucidate the factors affecting the switching day, we investigated the temperature that wasps experienced in the preceding period. For the temperature, the meteorological data from Sanda, Hyogo Pref. (the nearest weather-monitoring station to the present investigation site) were used (Japan Meteorological Agency: http://www.data.jma.go.jp).

Figure 4a shows the relationship between the average temperature from July 23 to August 1 (the 10-day) or from July 19 to August 1 (14-day) period before the switching day and the switching day in each year (see also Supplementary Table S15). Note that the 10-day average temperature is calculated from the 10-day cumulative temperature divided by the 10-day (days) and 14-day average temperatures in the same manner. Figure 4a indicates that there was a very high correlation between them (10 days: r = 0.96, t = 4.92, p = 0.03; and 14 days: r = 0.995, t = 14.9, p = 0.004). The percentage of overwintering eggs was thus negatively correlated with the preceding cumulative temperatures that the female experienced. This correlation indicated that this wasp shows increased voltinism from bivoltine to trivoltine when the cumulative temperature is high (i.e., in a hotter summer). This high correlation suggested that overwintering is determined by a female herself when she lays an egg. This phenomenon, wherein the temperature experienced by a female influences the induction of diapause in her offspring, is known in some hymenopterous insects, e.g., Trichogramma²⁷. There was a high correlation period in mid- to late July (Fig. 4b, Supplementary Table S16), indicating that the timing of switching physiological conditions of female wasps is dependent on the average temperature in this critical period. To confirm whether temperature conditions in the field practically influence the life cycle of D. sperconsus, further studies will be needed.

The emergence days of the overwintering generations were clearly different among years: most wasps emerged before May 1 in 2014 and 2015, while most wasps emerged after May 10 in 2013 and 2016 (Fig. 2). April mean temperature in Sanda, Hyogo Pref. was higher in 2014 (13.7 °C) and 2015 (14.1 °C) than in 2013 (11.8 °C) and 2016 (12.8 °C) (Japan Meteorological Agency: http://www.data.jma.go.jp). Thus, such higher air temperatures during the post-diapause period in 2014 and 2015 may have triggered the earlier emergence of the overwintering generations.

There was up to a two-month-duration between the spring emergence period (overwintering wasps in the laboratory: Fig. 3a) and the initial nesting period (wasps in the field: Fig. 3b). One of the reasons for such a long pre-nesting period of the overwintering wasps is that the overwintering wasps indoors emerged much earlier than those in the field, because the temperature condition indoors was warmer than that in the field. If it is the fact, this period may be actually shorter in the field than indoors. Another reason for the long-delayed oviposition may be due to the loss of energy during the winter; these wasps may have to collect energy and nutrients for egg maturation greatly. In fact, in some spider wasps, we often observed females hunt spiders solely for their own consumption (sting the spiders, masticate them with their mandibles, and ultimately abandon them in situ)²⁸. We need further studies to determine when overwintering wasps emerge in the field and what physiological conditions are necessary for egg maturation of overwintering wasps.

We integrated all these findings into a schematic illustration showing the life cycle of D. sperconsus in the present population (Fig. 5). This is the first record of the life history schedule of a spider wasp based on the consecutive daily surveys (Figs. 2, 3, 4).

Nesting activity

Cell productivity per day

The results of the consecutive daily investigations from 2014–2016 showed that 68 canes (2.7%; 68/2565*100) were utilized by Dipogon sperconsus among all 2565 canes installed in 2014 to 2016 (Supplementary Table S1 and S17). We also counted how many cells were constructed in a day: Out of a total of 68 nests, a single cell/day was found in 39 examples; two cells/day in 27 examples; three cells/day in seven examples; and four cells/day in two examples (Supplementary Table S17). Thus, the wasps constructed on average 1.63 cells/day (1–4, SD =  ± 0.77 cells/day). We should note that some nests were already found with one or more cells at the time of the weekly routine surveys. We excluded these records from the above data because we could not determine the starting dates for the analysis of cell production (Supplementary Table S17). This result was comparable to the three cells constructed in a single day by D. sayi sayi².

Prey spider species and sizes

One hundred and two spiders were identified as D. sperconsus prey over the four years. These comprised 74 coelotids, 21 agelenids, 5 segestriids and 2 thomisids (Table 3). The total of the former two occupied 93% of all samples.

For the coelotid spiders, 40 females and 34 males were used as prey, which shows that there was no significant sex bias in prey (z = 0.70, p > 0.1). Among the 40 coelotid female spiders, the sex ratio of wasp eggs was even: 20 female wasp eggs and 20 males. However, the female spiders on which female wasp eggs were laid were significantly greater in cephalothorax width than those on which male eggs were laid (t = 3.98, p < 0.001; Table 3). When male spiders were considered, significant more female eggs were laid than male eggs (z = 3.09, p < 0.01). The male spiders on which female eggs were laid were also significantly larger in cephalothorax width than those on which male eggs were laid (t = 4.61, p < 0.001). In other families of spiders, there was also a tendency for the spiders bearing female eggs to be larger than those bearing male eggs, but the differences were not significant (Table 3). These results indicated that a female wasp lays female or male eggs selectively depending on prey spider size. This habit is also recognized by an ichneumonid ectoparasitoid, Zatypota albicoxa (Walker), parasitic on Parasteatoda tepidariorum (L. Koch)²⁹.

Unutilized prey spiders

Occasionally trap nests included cells with a prey spider but without a wasp egg (“N” in Supplementary Table S17). These examples totaled 103 cases (6 in 2013, 12 in 2014, 32 in 2015 and 53 in 2016), which occupied 16.5% (103/623*100) of all cells. Apparently, these were not due to wasp death immediately after prey carriage because all of the cells containing a spider without an egg were partitioned or closed. The frequency of such cells tended to increase in the periods when many cells were constructed (coefficient of correlation between these factors per 10 days: r = 0.69, p < 0.001), but the reason for this was unknown.

Comparison with other species

As stated in the introduction, most of the tube-nesting species in Pompilidae belong to Auplopus and Dipogon^2,3. The nesting behavior of both genera, however, are fundamentally different. Species of Auplopus build barrel-shaped mud cells in series in tubes (building type)^1,30, while species of Dipogon construct a series of cells that are partitioned and closed by stuffing mud particles, sawdust and other materials (renting type)^1,10. The effects of the difference on wasps’ survival are still not clear.

Fragmentary data on the number of cells in a nest, the length of each developmental period and the sex ratios have been reported in some pompilid species^2,8,9,16. However, precise information on nesting ecology is still lacking, e.g., seasonal changes in the numbers of newly emerging adults and voltinism. The current report presents the first detailed data on the nesting ecology that can be used for the comparisons with other species in future studies.

Source: Ecology - nature.com