Introduction

Social wasps seem to rely on strictly annual colony cycles at high latitudes and altitudes, requiring a stage adapted to unfavorable seasons. This seems self-evident, considering the life cycle of Vespinae or Polistes. In general, newly emerged females of temperate-zone species seem to have three main possibilities: be a worker now, be a foundress next year, or (if it cannot) become a worker. Females of tropical species that have long colony cycles have one additional option: replace a reproductive as an egg layer on the former nest. In the tropics, first-born daughters need not be workers, later-born daughters and egg layers need not be foundresses, and foundresses need not be egg layers. In fact, these hypothetical routes are derived from the biology of some tropical Polistes, especially the fate of females that congregate to pass through unsuitable conditions (West-Eberhard 1969).

Winter aggregations, composed of hibernating queens, have been recorded for temperate-zone Polistes (West-Eberhard 1969). In the subtropics, a comparable “hibernation” phase is found in the paper wasp Polistes versicolor (Gobbi 1977; Gobbi and Zucchi 1980; González et al. 2002, 2004), which engages in facultative winter aggregations. A similar behavior has been observed in Costa Rica in Polistes instabilis, whose females form resting congregations at high altitude, passing the winter in “cold storage” (Hunt et al. 1999).

Polistes versicolor distribution ranges from Costa Rica to Argentina (Richards 1978). In colonies studied in southwest Brazil, the colony cycle lasts from 3 to 10 months (Gobbi 1977). New colonies are always founded by lone queens, occasionally followed by associations. Foundresses may come from these aggregations (Gobbi and Zucchi 1980). According to (Gobbi 1977), colony size varies from seven (foundress associations) to nearly 100 females (mature colonies). In this study, we describe a phenomenon whereby body size increases with the approach of an unfavorable season in the tropics, which is comparable to the increase documented in temperate-zone Polistes (West-Eberhard 1969; Sullivan and Strassmann 1984).

Materials and methods

Between 1974 and 1975, 22 aggregations were collected in Ribeirão Preto, São Paulo State (21°11′ S, 47°48′ W; altitude 621 m), southeastern Brazil. Some aggregations were found at their beginning, allowing us to know the approximate initiation date. Other aggregations were not collected but they were observed to verify females’ fate. Twenty-four foundress associations (1974/1975/1977) were collected after the aggregation period. All individuals (n=504) were fixed in Dietrich’s solution, preserved in 70% alcohol, and later dissected.

To compare females from aggregations with foundresses, we standardized the collected data according to size, wing wearing, ovarian development, and fatty tissue. The individuals were grouped in eight size classes, based on wing length, in millimeters: l=7.8–8.1; 2=8.3–8.6; 3=8.8–9.1; 4=9.3–9.6; 5=9.8–10.1; 6=10.3–10.6; 7=10.8–11.1; 8=11.3–11.6. Wing wear was used as a correlate to time spent foraging: four categories were defined as shown in Fig. 1. For fatty tissue amount, four categories were defined (based on visual estimate) as follows: a=25%; b=25–50%; c=50–75%; d=75–100%. These categories were scaled to females with the most fatty tissue (=100%). Other females with less fatty tissue were proportionally categorized. Ovarian development and insemination were also examined. For each female, the spermatheca was removed and placed on a glass slide in a 1:1 solution of glycerin and 70% alcohol. The presence of sperm cells was assessed using a light microscope. Five patterns of ovarian development were then defined as shown in Fig. 1.

Fig. 1
figure 1

Grades of ovarian development in Polistes versicolor. a Small ovaries, with filamentous ovarioles bearing no visible oocytes. b Small ovaries, bearing oocytes under development. c Large ovaries, bearing nearly mature oocytes located in the base of ovary. d Large ovaries, well-developed oocytes. e Large ovaries, bearing visible reabsorbed. Scale bar 1 mm. 1 to 4 indicates increasing patterns of wing wearing in Polistes versicolor

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To estimate body size variation, 340 females were collected from colonies in different stages of development, and 17 body parts were measured (Fig. 2). Also, hamuli number was counted. Groups were defined for the analyses based on direct observations performed by Gobbi (1977): 1—aggregations; 2—foundresses; 3—first batch of emerging workers; 4—queens; 5—workers. Data were log-transformed, and differences for each variable were tested using Bonferroni-adjusted t tests after ANOVA analyses. A stepwise discriminant analysis (Rao 1973) was performed to identify the most significant contributors for caste distinction. Later, the most informative characters were plotted for caste discrimination. Wilks’ lambda values were used to infer the individual contribution of each variable to the model. To verify the efficiency of the test, a classification matrix test was used to check the number and percentage of correctly classified cases in each group. This test compares the actual data with predicted results based on the discrimination model. Canonical scores were also evaluated to identify the contribution of each root in the discrimination model.

Fig. 2
figure 2

Representative measures for morphometric analyses of this paper: head width (HW), head length (HL), maximum and minimum interorbital distances (IDx and IDm, respectively), gena width (GW), eye width (EW), pronotal width (PW), mesoscutum length and width (MSL and MSW, respectively), mesoscutellar length (MTL), mesosomal height (MSH), alitrunk length (AL), basal and apical widths of gastral tergite II (T 2 BW and T 2 AW, respectively), length and height of gastral tergite II (T 2 L and T 2 H, respectively), partial forewing length (WL), namely, cubital cell length

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Results

Aggregations and foundress associations

At the studied area, aggregations in P. versicolor started in early March, before winter, lasting until mid-August. In numbers of females, an aggregation varied from six to 80 individuals, and males stayed for a few days, being forced to leave by the females.

In both aggregations and foundress associations, most individuals present less wing wear (Fig. 3). Most females have a large amount of fatty tissue (class d, Fig. 4.1) in both aggregations and foundress associations. The only difference is the greater number of females in class c than in class b for aggregations, while foundress associations show the opposite pattern.

Fig. 3
figure 3

Indication that females in aggregations (A) and foundress associations (F) of Polistes versicolor present less wing wear in Polistes versicolor. 1 to 4 indicate progressive age

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Fig. 4
figure 4

Size classes of females in aggregations (A) and foundress associations (F) of Polistes versicolor. 1 Preponderance of females with more fatty tissue of Polistes versicolor. 1 to 8 are size classes. a–d Progressive accumulation of fat tissue. 2 Size and insemination in aggregations and foundress associations. 3 Indication that in aggregations, females have less ovarian development than those from foundress associations. A–D Progressive ovarian development. (K) indicates ovaries in absorption state. 1 to 8 are size classes

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In many females, insemination apparently occurs before the participation in aggregation (Figs. 3 and 4.2). In aggregations, 75% of the females were inseminated, whereas in founder associations, 85% of the females were inseminated. Insemination was not restricted to the largest females (Fig. 4.2), even though the smallest females (class 1) were never inseminated.

In aggregations, most individuals present incipient ovarian development (patterns A and B; Fig. 4.3). In foundress associations, however, ovarian pattern C was predominant, with sizes similar to those of aggregations (Fig. 4.3). These findings indicate that females can develop their ovaries during aggregations. On the other hand, the presence of individuals with ovarian pattern K (with oocytes clearly reabsorbed) but apparently young (Figs. 1 and 4.3) suggests that they develop ovaries before the aggregation, in turn suggesting that young females may join an aggregation to await a better season (Fig. 4.3), instead of founding a new nest immediately.

Size variation among females

All body parts measured revealed differences among some of the groups (Table 1). In most cases, differences were due to aggregated females’ being larger than all other females and first emerging females’ being smaller than all individuals, which are expected due to the population dynamics of the species (Gobbi et al. 1993). In a few cases, there were differences among the other groups (foundress association, queens, and workers, Table 1). Multivariate statistics confirmed this result, as only 11 of 18 characters were used by the discrimination model. Wilks’ lambda values were around 0.35 (Table 2). Considering a range between 0 to 1, the variation can be useful in discrimination. Predicted vs observed classifications, based on discriminant analysis, show all a priori defined groups to have been correctly classified except foundresses (Table 3). Four canonical variables were extracted from the model (Table 4). Because the major variance may be obtained from the first variable (Table 4), only size is determining the observed variation (Fig. 5).

Table 1 First emerged females (FF), aggregations (A), foundress association (WA), queen (Q) and worker (W) means±SD, and one-way ANOVA analyses for each morphometrical variable in Polistes versicolor: head width (HW), head length (HL), maximum and minimum interorbital distances (IDx and IDm, respectively), respectively, gena width (GW), eye width (EW), pronotal width (PW), mesoscutum length and width (MSL and MSW, respectively), mesoscutellar length (MTL), mesosomal height (MSH), alitrunk length (AL), basal and apical widths of gastral tergite II (T2BW and T2AW, respectively), length and height of gastral tergite II (T2L, T2H, respectively), and partial forewing length (WL), namely, cubital cell length
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Table 2 Discriminant morphometric variables among first emerged females, aggregations, foundress association, queens, and workers in Polistes versicolor based on discriminant function analyses using the stepwise procedure
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Table 3 Classification matrix between observed and predicted classifications of first emerged females (FF), aggregations (A), foundress association (FA), queen (Q), and worker (W) after discriminant analysis in Polistes versicolor
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Table 4 Chi-square tests with successive roots removed after discriminant analyses in Polistes versicolor
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Fig. 5
figure 5

Discrimination among first emerged females (FF), aggregations (A), foundress association (FA), queens (Q), and workers (W) of Polistes versicolor using the first canonical score after discriminant function analysis

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Discussions

In aggregations, new queens are indisputably the larger females among the females compositing an aggregation. After new nests are founded, the first emerged females are the smallest individuals. Based on our data, the group formed by females from aggregations was the most robust (Table 4), and because most variations were restricted to the first canonical root (Fig. 5), the differences found here were exclusively size-related (Anderson 1958). In other words, there are no allometric growth changes as seen in highly eusocial polistines (Noll et al. 2004). The present data on aggregations in P. versicolor suggest that environmental changes may switch a colony toward the production of larger females, which are probably more capable of surviving a difficult season and starting a new nest, which is similar to what is seen in temperate-zone Polistes (West-Eberhard 1969; Sólis and Strassmann 1990; Dani 1994). In contrast to temperate-zone species, however, a foundress of P. versicolor may use fatty tissue as a source for egg production, as observed in P. fuscatus (West-Eberhard, personal communication).

Ecologically, P. versicolor is similar to temperate-zone species such as Polistes fuscatus or Polistes dominulus rather than other tropical species such as Polistes canadensis because although seasonal conditions are not drastic in terms of temperature, in southeast Brazil, there is a pronounced dry season (Koeppen 1931).

The fact that most females from aggregations were relatively large, and possibly young, might be taken to indicate synchronicity in the production of new females that will join the aggregation in P. versicolor. Most females may join the aggregations with undeveloped ovaries, but most females from foundress associations had their ovaries well developed (Fig. 4.3). It is plausible, therefore, that ovarian diapause is absent in females in foundress associations. In this way, foundresses would be able to start new nests and lay eggs immediately after they leave the aggregation. In contrast to hibernating queens in the temperate zone, several noninseminated females join the aggregations, having been mated during this period. Similar to hibernation, there is an accumulation of fatty tissue before the resting period as occurs before temperature decrease in temperate zone (Spradbery 1973). This fact, however, is probably a character related to the seasonally unfavorable conditions (Wenzel 1992).

A peculiarity of the P. versicolor pattern is that an aggregation may start in a very broad interval, from March to August, and founders do not leave the aggregation at the same time (Gobbi 1977; Gobbi and Zucchi 1980). Consequently, new foundations occur in different periods. Because only larger females (above size-class 4; Fig. 4.3) presented higher ovarian development (pattern D), it is possible that size (or something correlated with size) might be a restricting factor for attaining queen status in P. versicolor. Queen size seems to be important in competitive skill in societies headed by multiple queens (Reeve 1991). Dominant queens may exhibit greater ovarian development (Queller and Strassmann 1989) and may be larger than subordinate females (Sullivan and Strassmann 1984). Such patterns stated above suggest that body size is probably determining the differential survivorship of the larger queens.

In conclusion, aggregations represent an alternative for the traditionally accepted process of colony foundation (West-Eberhard 1969; Spradbery 1973), in which colonies are initiated only by new queens as soon as they leave the former nest. Consequently, aggregation in tropical Polistes is a characteristic that gives females a choice between starting a new nest or waiting until favorable weather conditions.