Insectes soc. 44 (1997) 15 – 21 0020-1812/97/010015-07 $ 1.50+0.20/0 © Birkhäuser Verlag, Basel, 1997
Insectes Sociaux
Research article
Nesting biology of the mangrove mud-nesting ant Polyrhachis sokolova Forel (Hymenoptera, Formicidae) in northern Australia M. G. Nielsen Institute of Biological Sciences, University of Aarhus, DK-8000 Aarhus, Denmark e-mail:
[email protected]
Key words: Mangrove, ants, Polyrhachis sokolova, nest, inundation, foraging. Summary The nest sites of the mud-nesting ant Polyrhachis sokolova were studied in Darwin Harbour mangroves. They were found from the Ceriops tagal zone to the Rhizophora stylosa zone at elevations ranging from 7.22 to 5.99 meters above the lowest astronomical tide (LAT), which means that the nests were inundated in 13–61% of all high tides and for durations of up to 3.5 hours. The nest structure was studied by excavating nests and making a cast of the galleries using polyurethane foam. The nests were quite extensive, normally with two elevated nest entrances and galleries down to depths of 45 cm. The loose soil particles at the nest entrances collapsed when the tide reached them and formed a stopper which prevented water from intruding into the nest. In this way, the galleries remained dry during high tide. The ants showed a clear swimming or “walking on the surface” behaviour when they returned to the nest just before the entrance collapsed and during ebb. The tolerance of the ants to submergence was tested in the laboratory, with 50 % mortality after 11 hours submergence in seawater at 23 °C, and only 3.5 hours in water at 33 °C. Therefore, the nesting behaviour with trapped air in the galleries is necessary for survival in these environments.
Introduction Ants are reported to inhabit tidal areas in various localities throughout the world, although very few investigations have been carried out on the nesting biology of these species. Nielsen (1981, 1986b, 1992) studied the ant Lasius flavus Forst on tidal meadows in Denmark, where the ant domes are inundated irregularly a few times each year. Similar studies have been carried out on the same species by Boomsma and Isaaks (1982) in The Netherlands. Yensen et al. (1980) investigated ant fauna on the tidal zone in the Gulf of California, where they found three species, Brachymyrmex depilis Emery, Forelius pruinosus analis (E. André) and Forelius sp. (undescribed), whose subterranean nests were flooded regularly. Majer and Delabie (1994) studied the ant communities in annual inundated forests in the Brazilian Amazon.
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Studies on mangrove ant fauna are very rare, with most of the information coming from broader investigations of insect fauna in this habitat and showing that the soil-nesting ant Polyrhachis sokolova Forel nests in the wettest habitats (Kohout, 1988; Ellway, 1974; De Baar and Hockey, 1987, 1993; De Baar, 1994). Richard Noske (unpublished) and Roger Clay (unpublished) studied ant fauna in mangrove habitats in Darwin Harbour, N.T., Australia, and found a total of 14 species. The species investigated in this study is considered to be P. sokolova, although there are slight morphological differences between these populations and these in Queensland (R. Kohout, pers. comm.). This species is distributed throughout the mangroves in Queensland and the northern coast of Australia. The aim of this study was to investigate the nesting biology of P. sokolova in order to elucidate its survival mechanism in this regularly flooded environment. Several nests were excavated and a cast of one nest was made using polyurethane foam. Further, field observations of the behaviour of the ants before and after flooding were made. Finally, a series of laboratory experiments were conducted to determine the ants’ tolerance to submergence.
Study site The field investigations were carried out near Palmerston in Darwin Harbour, Northern Territory, Australia (12°30′S 131°00′E). The mangrove community is typical for this region of Australia, with a high diversity of more than 30 species of trees (Wightman, 1989). The distance from the landward edge of the mangrove to the seaward edge is approximately 500 meters. There is a clear zonation of the main mangrove tree species with a 2–5 meter tall growth of Ceriops tagal near the dry edge of the mangrove. The following zone is dominated by Avicennia marina shrubs or trees with a height of 2 –4 meters. A dense and homogenous zone of Bruguiera sp. is followed by the final Rhizophora stylosa zone, where the trees reach heights of 10–15 meters. More detailed descriptions of the Darwin Harbour mangrove community are given by Hanley (1992) and Hutchings and Saenger (1987). The soil is heterogeneous, partly due to the very high density of digging craps, but the very high content of clay and silt make it only slightly water-permeable.
Methods Nests of P. sokolova were located by following foraging workers back to nest entrances. Ten nests distributed from the dryer Ceriops tagal zone to the wet Rhizophora stylosa zone were excavated to varying degrees in order to investigate the gallery structure. A cast of a typical P. sokolova nest was made using polyurethane foam. The cast was made by placing two plastic tubes deep in the nest entrances and then covering the entire surface of the nest with a 2-cm layer of plaster of paris, so that the nest could withstand the pressure needed to force the foam into the deepest galleries. After the plaster of paris had hardened, two cans of 500 ml polyurethane foam were emptied under pressure through the plastic tubes
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into the nest. The following day the soil and the very dense root system around the nest were sawed into 10-cm thick slices, which were brought back to the laboratory for cleaning. The maximum water level covering the nests was measured using simple water level equipment at two nests, and by manually measuring the depth of water over the nest sites during a high tide of known amplitude. The frequency and duration of inundation of the nests were estimated by water-level readings carried out by the authority of the Port of Darwin. A series of drowning experiments were conducted to determine the ants’ tolerance to inundation. The ants used in this experiment were collected in the field using a small vacuum cleaner. Ten to 30 individuals were sucked up into small gauze bags. The bags were then transported to the laboratory, where they were totally immersed in seawater. The experiments were carried out at 23 °C and 33 °C using 315 and 226 ants, respectively. Each sample had at least 30 individuals. The bags were retrieved at intervals ranging from 0.5 to 15 hours, and the ants were counted and placed on filter paper in small 100-ml plastic containers. The numbers of surviving ants were counted again during the following 24 hours.
Results and discussion Nest inundation Nest elevations ranged from 7.22 meters to 5.99 meters above the lowest astronomical tide (LAT). The official data on the tides in Darwin Harbour show that the nests at the highest elevation are submerged by 13% of the high tides for up to 125 hours, whereas the lowest nests are submerged by 61% of the high tides for periods of up to 3.75 hours. Observations during the flood revealed that foraging workers often ran or swam on the water surface in order to reach the nest entrance before it was submerged. When the water reached the nest entrance, loose soil particles collapsed and formed a stopper, sealing the entrance for water. When the water withdrew, the ants reopened the entrances as soon as they were above the water level. The ants resumed foraging before the soil was dry, and used the same running or swimming behaviour to cross wet areas during their foraging on the mud surface. Ants can be influenced by inundation in a number of different ways. This behaviour is reflected in the way they avoid drowning. For example, the annual inundation of the Amazon region (Adis, 1984; Majer and Delabie, 1994) leaves the forest floor flooded for 5–6 months. The only way ants can survive these conditions is to move their nests up in the trees. Adis (1982) reports that leaf-cutting ants of the genus Acromyrmex can swim or “walk” on the water surface during foraging in the flooded periods. This resembles the swimming behaviour observed for Polyrhachis sokolova when they returned to the nest at incoming tide in the present study. In northern Europe, tidal meadows are often inundated for up to several days during the winter season. The dominant ant species, Lasius flavus, lives in plantcovered sand nests, which give no protection against infiltration of seawater. These ants, the larvae, and their aphids are all submerged during the inundation (Nielsen,
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1981). In the present study, the nests of Polyrhachis sokolova were frequently flooded at predictable times. The behaviour of these ants shows that they have adapted to these conditions and have developed an efficient utilization of the available foraging periods. The restrictions enforced on foraging periods by flooding may be compensated for by living in the very productive part of the mangrove, where there appears to be only limited competition from other ant species. The conditions on the intertidal halophyte-covered mud flat in Mexico where Yensen et al. (1980) studied three soil-nesting ant species are also very similar to those in the present study. Some of the Mexican nests were covered by water 149 times a year for up to 3.5 hours. Nest structure All nests of P. sokolova were found in the mud, often with two nest entrances elevated above the mud surface between the trees and close to the roots. Most of the entrances were surrounded by a crater of particulate soil, which the ants excavated from the nest. The extent of the nests can be more than 100 × 50 cm. The galleries were most abundant in the upper 20 cm of the mud, but reached depths of up to 45 cm. Figure 1 shows a section of the cast 40 cm from a tree. It is evident that the majority of small chambers are situated around the highly developed root
Figure 1. Polyurethane-foam cast of a Polyrhachis sokolova nest from the mangroves. A cross section 40 cm from the centre of the nest with an intact root system; the measuring tape indicates the mud surface
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systems. Galleries connecting the main compartments of the nest were found immediately under the soil surface. Alates, workers, and brood were found throughout the entire nest. The walls of the nest chambers all consisted of very smooth clay. The galleries were not covered in silk, as in the case with some of the other members of the Polyrhachis subgenera (Hölldobler and Wilson, 1983). The cast and the excavation of P. sokolova nests showed that the galleries covered a considerable area with small tunnels connecting the main parts of the nest. This structure has the advantage that intrusion of water in one part of the nest does not necessary mean that the whole nest will be flooded. During excavation at high tide, it was found that all chambers contained air, even when situated below the water surface. During flooding, air could be squeezed out of the submerged nest by treading on it. The dense root system in the nests provides a structural support to the galleries, which may be of importance when nests are covered with up to two meters of water. There was no evidence of seeds in the nests, so it seems doubtful that P. sokolova collected Avicennia seeds as reported by Wightman (1989). The observed food items the ants brought back to the nest covered a very broad range: small Decapods, Amphipods, Lepidoptera larvae, Hemiptera, and some unidentified insect fragments. The very extended gaster of some of the returning workers indicated that they also collect liquid food, and they have been observed feeding on bird excrements. Drowning experiments The survival curves (Fig. 2) follow typical toxicological dose-response curves. The time in which 50% of the P. sokolova ants were killed (LT50 ) was 11 and 3.5 hours at 23 °C and 33 °C, respectively.
Figure 2. Percent survival after submergence in seawater at two temperatures for workers of Polyrhachis sokolova
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The drowning experiments also showed that the survival rate during submergence is strongly dependent on temperature. The ratio between the time in which 50% of the ants were killed at 33 °C and that at 23 °C was equivalent to a factor of 3.1, indicating that the time the ants can withstand submergence increased with a factor 3.1 for each 10 °C decrease in temperature. This temperature-dependent survival rate also indicates that survival depends on the metabolic rate of the ants and that the cause of death is asphyxiation. Thus, the factor 3.1 reflects the influence of temperature on metabolism and is within the range of the expected respiratory Q 10 for ants of this size (Nielsen, 1986a). Similar drowning experiments with Lasius flavus showed that workers could survive 120 hours in 5 °C seawater (Nielsen, 1981). Extrapolation of the values for P. sokolova to 3 °C shows that they should survive 106 hours given very similar submergence tolerance for the two species. The slight difference may be caused by a relatively higher rate of oxygen diffusion into the smaller Lasius flavus. The hairy surface of P. sokolova can capture and hold an air film, which probably can extend the submergence time limit for this species in comparison to other species. However, their tolerance to submergence is still so low that the species cannot survive in this environment without trapping air in the galleries of the nest. Acknowledgements This study was supported by a grant from the Danish Natural Science Council. I would like to thank the Tropical Ecosystem Research Centre at CSIRO in Darwin for providing facilities during my stay. I am also very grateful to Dr. Alan Andersen from CSIRO at Darwin and Dr. Jonathan Majer from Curtin University of Technology, Perth for their criticism and linguistic improvements to the manuscript. Finally, I would like to thank Dorthe Birkmose for her enthusiasm throughout the fieldwork despite the temperature, the humidity, the number of stinging insects, the mud, and the smell that made the work a “little” uncomfortable.
References Adis, J., 1982. Eco-entomological observations from the Amazon: III. How do leafcutting ants of inundation-forests survive flooding? Acta Amazonica 12:839 – 840. Adis, J., 1984. Adaptations of arthropods to Amazonian inundation-forests. In: Ecology and Resource Management in the Tropics (K.C. Misra, Ed.), Bhargave Book Depot Chowk, Varansi, India. 1:9–40. Boomsma, J. J. and J.A. Isaaks, 1982. Effect of inundation and salt on the survival of ant in a sandy coastal plain. Ecol. Entomol. 7: 121 – 130. De Baar, M. and M. Hockey, 1993. Mangrove Insects. Australian Science, Autumn Issue, 44 – 45. De Baar, M. and M. Hockey, 1987. Mangrove Insects. Wildlife Australia 24: 19 – 21. De Baar, M., 1994. New records, food plants and life-history notes for lycaenids (Lepidoptera) and formicids (Hymenoptera) (abstract). Entomol. Soc. Queensland. News Queensland. News Bulletin 22: 50–52. Ellway, C. P., 1974. An ecological study of Corio Bay, Central Queensland. Habitat. Environmental Survey prepared for Capricorn Coast Protection Council. Hanley, J. R., 1992. Current status and future prospects of mangrove ecosystems in North Australia. Conservation and Development Issues in North Australia. (Y. Moffat and A. Webb, Eds.). Hölldobler, B. and E.O. Wilson, 1983. The evolution of communal nest-weaving in ants. Amer. Sci. 71:490–499.
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Hutchings, P.A. and P. Saenger, 1987. Ecology of Mangroves, University of Queensland Press, St. Lucia. Kohout, R.J., 1988. Nomenclatural changes and new Australian records in the ant genus Polyrhachis Fr. Smith (Hymenoptera: Formicidae: Formicinae). Men. Qld. Mus. 25: 429 – 438. Majer, J.D. and J.H. C. Delabie, 1994. Comparison of the ant communities of annually inundated and terra firme forests at Trombetas in the Brazilian Amazon. Insectes Soc. 41: 343 – 359. Nielsen, M.G., 1981. The ant fauna on the high salt marsh. (C. J. Smith et al., Eds.) In: Terrestrial and Freshwater fauna of the Wadden Sea area 10: 68 – 70; Leiden/Netherland. Nielsen, M.G., 1986a. Respiratory rates of ants from different climatic areas. J. Insect Physiol. 32 :125–131. Nielsen, M. G., 1986b. Ant nests on tidal meadows in Denmark. Entomol. Gener. 11:191 – 195. Nielsen, M. G., 1992. The nest building activity of Lasius flavus F. In: Biology and Evolution of Social Insects (J. Billen, Ed.). Leuven University Press, Leuven/Belgium. pp. 55 – 60. Wightman, G. M., 1989. Mangroves of the Northern Territory. Northern Territory Botanical Bulletin. No. 7. Palmerston, Conservation Commission of the Northern Territory. Yensen, N., E. Yensen and D. Yensen, 1980. Intertidal ants from the Gulf of California, Mexico. Entomol. Soc. of Amer. 73: 266–269. Received 22 February 1996; revised 5 August 1996; accepted 10 August 1996.
