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Notes on the Predation of an Aviculariine Spider (Araneae: Theraphosidae, Avicularia sp.) by Pepsis frivaldszkyi (Hymenoptera: Pompilidae) in Brazilian Amazonia Felipe N. A. A. Rego1,2, Cristina A. Rheims3,4 & Eduardo M. Venticinque2
1

Mestrado em Ecologia, Instituto Nacional de Pesquisas da Amaznia (INPA), Manaus, Amazonas, Brazil; 2Projeto Dinmica Biolgica de Fragmentos Florestais (PDBFF/INPA - Smithsonian), Caixa postal 478, CEP 69011-970, Manaus, AM, Brazil; 3Laboratrio de Artrpodes Instituto Butantan, Av. Vital Brasil 1500, CEP 05503-900, So Paulo, SP, Brazil; 4Departamento de Zoologia, Instituto de Biocincias, Universidade de So Paulo, SP, Brazil.

Abstract In this paper we present the first record of the predation of an aviculariine spider (Avicularia sp.) by a Pepsis frivaldszkyi wasp in a flooded forest in Central Amazonia. The transport of the spider host to the shelter is recorded and questions on the reproductive behaviour of parasitoid wasps are discussed. Introduction Towards the end of the eighteenth century, the Spanish naturalist, Don Flix de Azara, recorded, for the first time in South America, the behaviour of spider hunting wasps (Azara 1998). Later, in 1832, Charles Darwin recorded, in Rio de Janeiro, the duel between a wasp of the genus Pepsis Fabricius and a spider of the genus Lycosa Latreille (Darwin 1913). This interaction was then studied in greater detail by Jean-Henri Fabre, in the beginning of the nineteenth century (Fabre 2001). Although this behaviour has been known for quite a long time, records of wasps attacking spiders in nature are rare even though, considering the diversity of these two animal groups, these encounters occur frequently. To date, over twelve thousand species of hunting wasps are known to science. Some of these are specialized in the capture of spiders, in which they deposit their eggs. These hymenopterans spend most of their life cycle inhabiting other organisms, thus are called parasitoids. The family Pompilidae (Hymenoptera) includes over 4000 species of wasps which, during their larval stage, inhabit the interior of live spiders and feed on their tissue until the pupal stage (Fernndez 2000). Within Pompilidae, the parasitoid wasps of the genus Pepsis can reach up to a 9 cm body length, and are notorious for their ability to capture large sized individuals such as those spiders of the family Theraphosidae (Mygalomorphae) (Williams 1956). Approximately 100 species of Pepsis are known from the Neotropical region (Fernndez 2000), of which only females capture spiders. The males are in charge of searching for mates during their reproductive period. Adult Pepsis wasps are solitary, feed on nectar and are usually long legged and large. Their coloration is usually dark blue, but some species are known to exhibit a metallic appearance.

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Plate 1: Predation of a juvenile Avicularia sp. by Pepsis frivaldszkyi - photo by Felipe Rego.

Plate 2: Pepsis frivaldszkyi using its mandibles to hold the immobile spider and drag it towards the shelter - photo by Felipe Rego.

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The attack Aspects of the reproductive behaviour of Pompilidae wasps are common to other species and can illustrate, in general, the encounters between the wasps and their prey. Female Pepsis forage close to the soil by means of quick, short and levelling flights. The encounters can be random or the result of an active search, by which the wasp is capable of finding the prey even in shelter (revised by Coelho 2000). Once the host is located, the combat, of which the wasps are usually the winners, begins. The spiders brandish a pair of chelicerae distally armed with fangs. Nevertheless, these fights are usually brief. The wasp prevents the spiders counterattacks by maintaining a safe distance, using their long legs and spines. Using their sting, the wasp injects a paralyzing substance several times into the soft tissue of the spiders cephalothorax. A final sting is given to the mouth region putting the spider to sleep (Costa et al. in press). Completely immobilized and defenceless the spider is unable to prevent the wasp from depositing an egg on its abdominal surface. The larva that emerges from this egg will consume the spider slowly until its death (Petrunkevitch 1926). Some hunting wasps complete their reproductive role once the egg is laid. Others however, transport the host to a safe place in order to guarantee the development of their offspring. In this paper the transport of a spider of the genus Avicularia Lamarck, 1818 to the shelter of a Pepsis frivaldskvi Mocsry, 1885 is described for the first time. The record of both species interacting in nature is also recorded for the first time, and was used as a basis for a discussion on reproductive behaviour of spider hunting wasps. Methods In November 2003, at approximately 15:00h in the municipality of Itacoatiara (AM), Brazil (315S, 5932W), the predation of a juvenile Avicularia spider by a P. frivaldskyi wasp was observed. This observation was made in a floodplain (vrzea) (Junk 1996), which is submerged to 1.5 m during the flood of the Rio Amazonas (the flooding peak typically occurs in July). Both specimens were collected with the aid of a plastic pot and the distance the wasp transported the spider was measured with a measuring tape. The specimens of P. frivaldszkyi and Avicularia were deposited in the collections of the Museu de Zoologia da Universidade de So Paulo (MZSP, S.A. Casari) and Instituto Butantan (IBSP, I. Knysak), respectively. Results Specimens Pepsis frivaldszkyi has a golden cephalothorax, metallic-blue coxae and semitransparent brownish wings (Plate 1). The specimen measured 5.4 cm (measured longitudinally, from the head to the end of the abdomen) and weighed 3.8 mg.

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Plate 3: Transport of Avicularia to shelter by Pepsis frivaldszkyi - photo by Felipe Rego.

Plate 4: Guateria olivaceae, the tree used as a shelter to place the spider. The arrow points to the place where the specimens were captured before entering the shelter - photo by Felipe Rego.
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Plate 5: Detail of the shelter between the roots of the Guateria olivaceae (Annonacea) tree. Here the spider would probably be buried alive and slowly consumed by the Pepsis frivaldszkyi larvae - photo by Felipe Rego.

The aviculariine spider was black ventrally, with orange scopulae and very long, light-brown hairs covering the dorsal surface of the abdomen (Plate 1). The spider weighted 4.8 mg and had a total length of 9.3 cm. We were unable to identify the spider to species level because, being a juvenile specimen, it did not present developed genital structures. Transport In the beginning of the observation, we were able to see the spider completely immobile, turned upside down on the forest soil. The spider was covered with ants and the wasp seemed to be biting its cephalothorax. The wasp promptly ingested the haemolymph that leaked from this region. This activity was frequently interrupted by short flights around the prey, producing a very high buzzing sound due to the intense vibration of wings. Approximately three minutes later, the wasp began to drag the spider by its legs, holding on to it firmly with its mandibles (Plate 2). Moving quickly and without a stop, the wasp showed strength and ability, while dragging the immobile spider uphill over dry leaves, small branches and roots (Plate 3). In less than five minutes, the wasp had

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dragged the spider over approximately 30 m in a straight line, to a cavity among the roots of a Guateria olivacea R.E.Fr. tree (Annonaceae, Plate 4). We believe that here the wasp would bury the live spider, which would slowly be devoured by the larvae (Plate 5). Discussion Most studies on the predation of spiders by wasps were carried out under laboratory conditions due to the fact that it is much easier to observe the development of larvae (Petrunkevitch 1926, Williams 1956, Punzo 1994a,b, Costa et al., in press). In the field, records of the reproductive behaviour of Pepsis wasps are restricted to attacks and the confinement of the hosts in shelters (Darwin 1915, Cazier & Mortenson 1964, Azara 1998, Fabre 2001). These records are useful to determine the prey capture method as well as to study the biology of these animals. Some species, such as those of the family Sphecidae, accumulate several small spiders in their nests and are capable of preying on an enormous variety of spiders and arthropods (Peruquetti & Lama 2003). Large sized individuals, such as those of the genus Pepsis, seem to be limited by the size of the host and thus, need to capture large sized individuals such as mygalomorph spiders. The size of the prey seems to have a role in determining the sex of the offspring. Larvae deposited on hosts that are at least six times heavier than their parents have a better chance of being females (Costa et al., in press). The weight ratio between the Avicularia sp. and P. frivaldszkyi was 6:1 and it is probable that, if a larvae had been deposited, it would have yielded a female. Location of the shelters We did not have the opportunity to observe P. frivaldszkyi attacking the aviculariine spider. Nevertheless, the transport of the spider to the shelter leads to some questions about the reproductive behaviour of this wasp. What caught our attention was the fact that the wasp did not hesitate in taking the shortest route (almost in a straight line) to the shelter. Thus, it is possible that the wasp already knew the location in which to place the spider. When we first saw the spider, it was already immobile and covered in ants, suggesting that the wasp temporarily abandoned it. It is probable that the wasp left the spider in order to either locate or verify the conditions of a previously selected shelter. Thus, the wasp was able to transport the spider using the shortest and quickest route, demanding less energy consumption. Nevertheless, there is always a risk of loosing the prey during this brief search for the shelter, and for this reason it is likely that oviposition occurs only after the spider has been safely transported and stashed in the shelter. Cost and advantages of transporting the prey to a shelter Pepsis fridavlskyi ingested the body fluids that leaked from the spider during the attack in order to recover some of the energy consumed during the duel. Reproduction is extremely energy consuming for pompilid wasps, from

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copulation to the transport of the host, and parental care reduces the chances of this energy consumption being useless. Nevertheless, some wasps attack the spiders inside their own refuges and turn these into shelters for their larvae (Costa et al., in press). By doing this, they do not have to transport the hosts to the shelter and reduce energy consumption. The larvae remain in these shelters for several months until they reach the adult stage, at which point their mandibles are developed enough to enable them to leave the refuge. Some species, such as Pepsis cupripennis Taschenberg, devour their hosts in less than three weeks, becoming pupae shortly after. Nevertheless, at least seven months are necessary for them to become adults (Costa et al., in press). Hunting wasp larvae (Sceliphron jamaicense Fabricius: Sphecidae) can be attacked by parasitoid flies (Eulophidae: Diptera) while inside the hosts (Genaro 1996) and some species (Evagetes Lapeletier, 1845 and Ceropales Latreille, 1796: Pompilidae) even consume and substitute the eggs previously deposited by other wasps (revised by Coello 2000). Thus, the confinement of the aviculariine spider in a nest acts as a physical barrier to enemy attack, increasing the survival chances of the offspring. In addition, spiders captured in open fields can be transported to a safe place for over 150 meters (Azara 1998), and this behaviour can be considered as maternal care. Acknowledgments We wish to thank Eduardo F. Santos for identifying the wasp and Paulo A. C. L. Assuno for identifying the tree species; Ana L. M. Albernaz for logistic and financial support during the field work and Valdenir A. Freitas for support in the field. We thank Fernando G. Costa for making available his in press paper and for his comments and suggestions on the initial versions of this manuscript.
Azara, F. 1998. Viajes por la Amrica Meridional. Buenos Aires, El Elefante Branco. Cazier MA, Mortenson MA (1964): Bionomical observations on tarantula-hawks and their prey (Hymenoptera: Pompilidae: Pepsis). Annual Entomology Society of America. 57: 533541. Costa, F. G., Prez-Miles, F. & Mignone, A. In press. Pompilid Wasp Interactions with Burrowing Tarantulas: Pepsis cupripennis versus Eupalaestrus weijenberghi and Acanthoscurria suina (Araneae, Theraphosidae). Studies on Neotropical Fauna and Environment. Coello, D. F. 2000. Los Pomplidos: un exitoso ejemplo de predoparasitismo. Revista Ibrica de Aracnologa (Boletn). 1: 7376. Darwin, C. 1913. Journal of Researches into the Natural History and Geology of the countries visited during the voyage round the world of H.M.S. Beagle, 11 ed., London, John Murray, p.3538. Fabre, J. H. 2001. More Hunting Wasps. Blackmask Online. http://www.blackmask.com/books29c/mhtgw.htm#1_0_3. Fernndez, F. 2000. Avispas Cazadoras de Araas (Hymenoptera: Pompilidae) de la Regin Neotropical. Biota Colombiana. 1 (1) 324. Genaro, J. A. 1996. Nest parasites (Coleoptera, Diptera, Hymenopteran) of some wasps

References

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and bees (Vespidae, Sphecidae, Colletidae, Megachilidae, Anthophoridae) in Cuba. Carribbean Journal of Science. 32 (2): 239240. Junk, W. J. 1996. General aspects of floodplain ecology with special reference to Amazonian Floodplains. In: Junk, W. (ed.). The Central Amazonian Floodplain: Ecology of a pulsing system. (Ecological Studies 126) Springer-Verlag, Berlin, Heidelberg, New York. Punzo, F. 1994a. The biology of the spider wasp, Pepsis thisbe (Hymenoptera: Pompilidae) from Trans Pecos, Texas. 1. Adult morphometrics, larval development and the ontogeny of larval feeding patterns. Psyche. 101: 229241. Punzo, F. 1994b. The biology of the spider wasp, Pepsis thisbe (Hymenoptera: Pompilidae) from Trans Pecos, Texas. 2. Temporal patterns of activity and hunting behaviour with special reference to the effects of experience. Psyche. 101: 243256. Peruquetti, R. C. & Lama, M. A. D. 2003. Notas sobre a socialidade e a biologia de nidificao de Trypoxylon (Trypoxylon) asuncicola Strand, 1910 (Hymenoptera, Sphecidae). Revista Brasileira de Entomologia. 47 (2): 297301. Petrunkevitch A. 1926. Tarantula versus tarantula-hawk: a study in instinct. Journal of Experimental Zoology. 42: 367397. Williams F. X. 1956. Life history studies of Pepsis and Hemipepsis wasps in California (Hymenoptera, Pompilidae). Annual Entomology Society of America. 49: 447466.

o0o Phantom Egg-sacs in Theraphosid Spiders Ray Gabriel Phantom egg-sacs are unusual in tarantulas and occur when unmated females produce egg-sacs for no apparent reason. As far as I can tell there is no explanation why they do this. In all the years I have been keeping and breeding spiders, I have had very few: 1996 Tapinauchenius plumipes, 1998 Megaphobema mesomelas, Psalmopoeus reduncus, and this year (2004) Tapinauchinus gigas and Poecilotheria smithi. Poecilotheria smithi (female 1) produced a phantom egg-sac on the 3rd March 2004, and a second on the 28th June 2004. This was quite surprising, but then she produced a third sac on the 8th October 2004. A second female P. smithi (female 2) also produced a phantom egg-sac on the 3rd October 2004. I have thought for some time that phantom egg-sacs are produced in response to specific environmental conditions (temperature, humidity, etc) in captivity. Both female P. smithi are housed in Custom Aquaria glass tanks 20x20x35 cm (LxBxH). Each has a 30 cm piece of bamboo tube set at an angle in 1012 cm of coir substrate and a water dish. Both spiders are fed fortnightly on adult black crickets (I do not feed unmated females as heavily as I do mated females). These tanks are kept in a large heated cabinet along with other female Poecilotheria spp.

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