Living in aggregations: theories and facts in the life of Hymenoptera

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1 Living in aggregations: theories and facts in the life of Hymenoptera Manuela Giovanetti*, Josep Daniel Asís** and José Tormos** *Università degli Studi di Milano, Dip. Biologia, Via Celoria 26, MILANO (ITALY) **Universidad de Salamanca, Dep. Biología Animal, Avda. Campo Charro s/n, SALAMANCA (SPAIN) ABSTRACT This research investigated the behaviour of a solitary wasp, Stizus continuus (Hymenoptera: Crabronidae) and its nesting preferences. Solitary wasps (also called sand wasps, digger wasps, groundnesting wasps) are less famous than their social relatives (honeybees, paper wasps, bumblebees), still their biology leaves many open questions that may help the debate on the evolution of sociality in insects. A main topic is related to nesting choices: females often form aggregations of nests, notwithstanding the fact that there is no collaboration among them. Moreover, encounters between nesting females end up with aggressive reactions. So why are nests build so close one to the other? Hypothesis deal mainly with two sorts of factors: the abiotic (type of soil, exposure, vegetation, solar radiation, etc.) and the biotic ones (parasite pressure, presence of other nesting females, mating system, etc.). Especially if analyzed at the same time and on the same population, abiotic and biotic factors may reveal in what circumstances their action is affecting the success of a female. The presence of a wellestablished aggregation of S. continuus near Valencia (Spain) and records on Nemka viduata (Hymenoptera: Mutillidae), a possible parasite of this species, grounded an excellent opportunity to investigate the relative importance of abiotic and biotic factors on the aggregated nesting habit of solitary Hymenoptera. INTRODUCTION Hymenoptera is a large order of insects, that includes wellknown arthropods such as ants, bees and wasps. When thinking about these animals, the first image we recall is of a crowded honey nest: each of us has at least one painful experience to report about the sting of these insects! Less known is the fact that individuals of many species live a solitary existence. In this case no crowded nest appears, but instead each female digs a subterranean tunnel or enlarges the natural hole in a twig or dead plant stem. Where nest density increases, we have what is called an aggregation. Why does an individual, that does not share with others the duties related to reproduction, decide to dig so close to already established nests, possibly having to deal with aggressions from neighbours? Several theories examine densitydependent nesting preferences and they are not mutually exclusive. Some deal with the distribution of key resource [2] [16] [23] [29]. These studies underline how each species presents specific restrictions for what concerns a suitable nesting area. This may justify the election of the same place by different individuals, the socalled limited substrate hypothesis. Other studies focus on factors as closed presence of relatives, parasite pressure, or mating systems [5] [20] [24]. For example, the presence of many individuals in a restricted area may reduce the outcome of some natural enemies by an active defense of the nests or by disturbing or confusing the parasites [8] [30]. Nesting in aggregations has also been considered as a demonstration of Hamilton's selfish herd hypothesis [9] [13] [27]. In other cases, aggregation was not related with parasite pressure [21]. Moreover, aggregation was related to a higher rate of parasitism [26]. Records exists on the ability of individuals to recognise neighbours among all the ones living in the aggregation [15]. A female performs more tolerant behaviours towards neighbours, while the aggressions may be very serious towards other individuals of the same species, as well as to parasites. The ability of including other females in a tolerated entourage is an important step to the evolution of group strategies and could have reasonably appeared in situations of aggregated nests. Females accepting the presence of other individuals belonging to the same species may evolve mutual tolerance and further on some kind of cooperation may arise among them [7], as observed in primitively social species. Such behaviours are of extreme importance, because they could represent the first step towards the evolution of truly social behaviours. Many nests of S. continuus, a solitary groundnesting wasp, have been constantly recorded in a sandy area at Dehesa del Saler (Valencia, East Spain) since 1981 [14]. On this population, some preliminary studies [1] reported observations on the nest structure and the way of

2 provisioning, noticing also that males showed a territorial behaviour. A very recent paper reports details on male behaviour [32]. Female wasps dig starting from the hard salt crust and their progression is recognisable by the sand accumulated on the soil surface. The nesting site has diverse microhabitats; small bushes form restricted areas of dense vegetation, surrounded by bare soil. Females are known to nest in both (Figure 1). have no wings and walk on the ground), are mostly external parasitoids of the larvae and pupae of ground nesting bees and wasps. Information on parasitic behavior of velvet ants is lacking. In some cases velvet ants were observed searching for possible host nests [11] [18], entering any burrow in the soil and spending from 10 seconds to 16 minutes inside it [12]. In contrast, other authors have noted few cases of searching behavior even after many hours of observation, but none the less found heavy parasitism on the host nests (up to 43% in an aggregation, [25] [4]). The activity of these parasites may be cryptic and/or delayed in relation to the host one [18]. The population of S. continuus at Dehesa del Saler is then a good subject to test the factors influencing aggregated habits, because of the simultaneous existence of microhabitat variation, significant parasite presence and aggregated nests. METHODS Figure 1: The sand removed from the subterranean nests is easy to recognize on the surface, also if the entrance is usually perfectly hidden. Plants form dense spots. A nest contains many cells, each of them provisioned with 48 prey. The prey, always grasshoppers, belong to at least three families: Catantopidae, Pyrgomorphidae and Tettigonidae [1] and are probably hunted in close areas. The female stings them, not killing the animal but paralysing it and consequently preventing any reaction. The paralysis lasts many days and the larva will then feed on a fresh provision. Figure 2 shows a female, excavating at the nest entrance while holding a prey under her body. Figure 2: A females entering her nest with a prey. The grasshopper is grasped by the legs under the wasp body. Nemka viduata (Hymenoptera: Mutillidae) is a possible parasite of this solitary wasp. It was observed investigating the emergence holes on the ground [14]. Velvet ants, as they are called because of the hairy appearance and the strong resemblance with ants (females Data were collected in the field during the wasp nesting season from June to October We mapped the nesting area, dividing it in squares (3m x 3m; n = 28) to facilitate precise location of nests. There were two discriminable microhabitats, further on called bare soil and under vegetation, that covered respectively 151 m2 and 101 m2. Bushes of Salicornia ramosissima (J. Wooods) and Sarcocornia fruticosa ((L.) A.J. Scott) were the plants that formed restricted areas of intricate vegetation. When a new nest was established, it was precisely located on the map. At the beginning of the season, 12 females, recently starting the activity, were individually marked with nontoxic dyes and their head width measured as an estimate of size. Unfortunately, in the middle of June a particularly strong rain stopped the wasps activity for more than a month. This catastrophic event (the nesting site was completely inundated!) destroyed the nests already begun and delayed the excavation of new ones. During this time, we carried out some behavioural observations in a close area, where we marked 28 females. Notwithstanding the inundation, the population did not definitively abandon the first site, returning to it when the soil dried up. We also moved back to this site when activity restarted, recording daily air temperature, air relative humidity, soil temperature (at 13 cm depth) and soil hardness for both microhabitats. New nests were precisely located for densityrelated analysis, 62 females individually marked and some of them observed for records on daily activity. At the end of the season, some nests (3 with entrances on bare soil and 5 under vegetation) were excavated in order to describe their subterranean structure and verify the reproductive success (brood cell contents) of the female nesting in different microhabitats. We decided to excavate few nests to reduce the consequences on the population, established in a protected area.

3 RESULTS ABIOTIC. We compared some microclimatic factors that may influence the wasp decision to nest under vegetation or on bare soil, as air temperature and relative humidity, soil temperature, soil hardness. We also verify nest distribution in the two microhabitats in two time periods of the season: at the end of August (recolonization after inundation) and at the end of September (end of the season). Under the vegetation cover, temperature and relative humidity of the air as well as temperature and hardness of the soil were, as expected, lower than on bare soil, the difference being statistically significant for each factor (see Table 3). The 40% of the area was covered by vegetation: 101 m 2 against the 151 m2 of bare soil. The first analysis refers to 129 nests (72 under vegetation, 57 on bare soil): a higher number of wasps nested under vegetation, the difference being significant (X2 = 13.44; P < 0.001). The situation was the opposite at the end of September. The 257 nests (61 nests under vegetation and 196 nests on bare soil) were distributed significantly different but with a higher number of females nesting on bare soil (X2 = 28.33; P < 0.001). Statistical Difference Air Temperature Wilcoxon Test, z=7.29, P < Air Rel. Humidity Wilcoxon Test, z=7.12, P < Soil Temperature Wilcoxon Test, z=7.58, P < Soil Hardness MannWhitney Test, U=22.0, P < Table 3. Abiotic factors as temperature, humidity and soil hardness compared for the two microhabitats (under vegetation and on bare soil). The difference between the two resulted significant for each factor. NEST DENSITY. At the end of August, the overall nest density was 0.51 nests per m2. At the end of September, the overall nest density was 1.02 nests per m2. A more precise estimation of nest density, from a biological point of view, is the one obtained from the Nearest Neighbour Distance (NND) analysis [31]: for each nest we calculated the distance of its nearest neighbour. In September, the average distance among neighbour nests was cm (range: cm; n nests = 257). In the entire area the NND value obtained was This value shows that there is a tendency towards an aggregated pattern, which is statistically significant (c = , P < 0.001). BIOTIC. We compared the biological characteristics of nests with the entrance on bare soil (3 nests) and the ones with the entrance under vegetation (5 nests). The comparison included: number of cells, location of cells, number of wasp (Stizus) pupae, number of parasite (Nemka) pupae, number of cells with rests (mortality due to reasons other than parasitism). We compared also the number of prey/day captured by females that elected the two microhabitats for nesting (number of observed females: 6 with nest entrance under vegetation, 5 on bare soil). X2 P value value Under vegetation Bare soil total n nests excavated 5 3 total n cells mean cells/nest mean Stizus pupae/nest mean Nemka pupae mean n cells with rests females observed mean prey/day (range: (range: ) ) Table 4. Differences exist, from a biological point of view, between the nests located in the two microhabitats. Notwithstanding this, there is no statistical significance. The only statistically significant result (Table 4) comes from the comparison on the number of cells: it was higher in nests under vegetation. A very interesting discovery regards the cell location: cells were always under bare soil, also for those nests with the entrance under vegetation. Table 4 reports also descriptive statistics and test results on the other factors. Some biological differences emerged, regarding the content of nests in the two microhabitats, but they were not statistically significant. Instead, females activity as number of prey collected per day was very similar for wasps that decided to start the nest under vegetation or on bare soil. Also comparing the head width of a sample of marked females (n = 58), no differences emerged: average head width of females nesting under vegetation was 4.97 mm (SD 0.23 mm), while the one of females nesting on bare soil was 4.92 mm (SD 0.23 mm). A new discovery concerns the presence and activity of

4 two parasites belonging to the family Mutillidae. Two different species were active at the same time at the site, with males looking for females while females were searching host nests. These species, Nemka viduata and Ronisia ghilianii, are quite similar in morphology. DISCUSSION Results are not unambiguous. There is a preference to initiate nests under vegetation cover when the nesting activity starts. Under vegetation both soil hardness and temperature are significantly lower. When progressing with the season, nest number increases in areas of bare soil. It is possible that some abiotic factors not measured during this study, as direct solar radiation on the digging animal, are responsible for the observed change in preferences of nesting individuals. All the nests with an entrance under vegetation had cells located under bare soil. The decision of initiating a nest under vegetation may be related to the easier conditions of excavation (softer surface [6], no direct radiation affecting the thermal balance of the insect [10]), while the location of the cells is probably dictated by the thermal conditions required for larval development. The digging performance of females may improve considering the advantage of working in optimal thermal conditions. This could explain the significant difference in the number of cells: a female may save time during the first phase of excavation, not having to stop during hot hours. There must be other factors inducing some individuals to nest on bare soil. A female could decide to nest on bare soil if radiation, at the moment of excavation, is not limiting digging activity. Once a female starts nesting at a certain spot, it seems to attract other females [17] [22]; in this study, the final nest distribution resulted significantly different from a random one. Among others, biotic explanations to prefer an aggregated habit may refer to: a) protection from parasites; b) mating system; c) advantages from the presence of other females. a) In our case, parasites affected equally all nests, independently from the location of their entrances. The ability of two species, Nemka viduata and Ronisia ghilianii, in distinguishing animals belonging to the same species and non, may also be effective in recognizing the host. It is possible that chemical cues are used by returning females to detect their nest entrances (usually perfectly closed) and the parasite may take advantage of them, too [3] [19] [28]. In this case, nest location in relation to microhabitat would be of no importance, while many close entrances could actually create confusion. Anyway, knowledge on the behaviour of these parasites is still too poor to infer their importance on nesting decisions. It will be also interesting to understand if there is direct competition between the two species on the host species (Stizus continuus) that we were studying. b) Given that in this species mating occurs at the nesting site at the moment of emergence, a high nest density may indicate good mating opportunities for the progeny. Males seem to detect the location of emerging females and often excavate the hard salt crust on the soil surface in order to get at them, at the same time helping females to emerge [32]. c) At the end of the nesting season, we observed some females attacking returning ones to steal the prey they were bringing back to their nest. Nesting close to other females may allow such a strategy when prey abundance decreases, minimizing the risk of been followed by the original prey owner by quickly entering one's own nest. At the end of the season it may be more effective locating the nest on the base of the actual density instead of taking account of microhabitat differences. This study highlighted the need of more comparative researches on species nesting in aggregation. Abiotic and biotic factors may respectively play a dominant role in different moments of the nesting season (or in different seasons), as it seems to be the case for Stizus continuus in Considering the peculiar conditions of the field season during which these data were collected, also a comparative analysis on this species during a longlasting (June September) nesting season would be interesting. The Spanish research group is following this line of research and more results will be, hopefully, available soon. AKNOWLEDGEMENTS This research was funded by the European Community, thanks to an Individual Marie Curie Fellowship (HPMF CT ) given to the first author. MG wishes to thank all the persons working at the Dep. Biología at Universidad de Salamanca for their cordial reception during her stay. We are also especially indebted to the Adjuntament de Valencia, Oficina Técnica DevesaAlbufera, that allowed us to work in a protected area, and to Dr. R. J. Paxton for comments on the first draft of this manuscript. REFERENCES [1] Asís J.D., Tormos J. & R. Jiménez, (1988). Contribution to the study of the biology of Stizus continuus (Hymenoptera: Sphecidae). Entomol. News, 99: [2] Brockmann H.J., (1979). Nestsite selection in the great golden digger wasp, Sphex ichneumoneus L. (Sphecidae). Ecol. Entomol., 4: [3] Cane J.H., (1983). Olfactory evaluation of Andrena host nest suitability by kleptoparasitic Nomada bees (Hymenoptera: Apoidea). Anim. Behav., 31: [4] Deyrup M. & D. Manley, (1986). Sexbiased size variation in velvet ants (Hymenoptera: Mutillidae). Florida Entomol., 69 (2): [5] Field J., (1992). Intraspecific parasitism as an

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