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Ant Predation and the Cost of Egg Carrying in the Golden Egg Bug: Experiments in the field

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Ant Predation and the Cost of Egg Carrying in the Golden Egg Bug: Experiments in the field OIKOS 89: 254–258. Copenhagen 2000 Ant predation and the cost of egg carrying in the golden egg bug: experiments in the field Arja Kaitala, Xavier Espadaler and Risto Lehtonen Kaitala, A., Espadaler, X. and Lehtonen, R. 2000. Ant predation and the cost of egg carrying in the golden egg bug: experiments in the field. – Oikos 89: 254–258. Golden egg bug (Phyllomorpha laciniata) females lay eggs on the backs of both female and male conspecifics. Bugs receive eggs voluntarily and involuntarily, and even when males carry eggs, many eggs are not fertilised by the carrier. Carrying the eggs of another individual is unexpected, particularly if egg carrying bears a cost in survival. We examined the predation risk associated with egg carrying experimentally in the field. P. laciniata individuals were enclosed with workers of one of two ant species, Pheidole pallidula or Cataglyphis piliscapus, which co-occur with the bug in the wild. Pheidole pallidula workers preyed on golden egg bugs and their eggs, but Cataglyphis piliscapus workers did not. In P. pallidula enclosures, golden egg bugs carrying larger egg loads were eaten first. These results suggest that golden egg bugs experience high predation pressure and that egg carrying increases the risk of predation. Due to the direct survival costs associated with egg carrying and the lack of relatedness between the eggs and the carrier, we suggest the golden egg bug as the first known intraspecific parasite in which parasitism is not related to active parental care. A. Kaitala, Dept of Biology, Uni6. of Oulu, Box 3000, FIN-90014 Oulu, Finland (arja.kaitala@oulu.fi).–X. Espadaler, CREAF Uni6ersitat Auto`noma de Barcelona, E-08193 Bellaterra, Spain.–R. Lehtonen, Dept of Statistics, Uni6. of Jy6a¨skyla¨, Box 35, FIN-40351 Jy6a¨skyla¨, Finland. Predation is an important selective determinant affect- female conspecifics (Jeannel 1909, Reuter 1909, Kaitala ing prey spatial and temporal distributions, host selec- 1996). Eggs do not survive in nature unless they are tion and social behaviour (for review, see Taylor 1984, carried because of predation by ants (Kaitala 1996; but Crawley 1992). The higher the risk of predation, the see Mineo 1984). Newly laid eggs are white but turn more individuals should act to avoid those risks. Be- golden and shiny after 3–6 d, making the bug highly havioural and morphological adaptations may evolve visible when carrying eggs. In most cases, eggs are not to reduce predation risk. For example, individuals may fertilised by the carrying male (M. Miettinen and A. avoid predators by being cryptic (Cott 1940, Endler Kaitala unpubl.). Individuals receive eggs both volun- 1988). However, adaptations directed against one tarily and involuntarily (Kaitala 1996, 1998, Kaitala predator may be of limited or no value in protection and Miettinen 1997), and in the laboratory males often from another predatory species whose search image accept eggs without mating with the female. All females differs (Endler 1988). Visually cryptic prey may never- carry eggs they have not fertilised. Copulating individu- theless be detected by chemical or other means. als seem especially unable to resist oviposition attempts The golden egg bug, Phyllomorpha laciniata Vill (Kaitala and Miettinen 1997). Egg carrying is theoreti- (Heteroptera, Coreidae), is a highly cryptic species cally problematic if the costs of carrying are higher (Cott 1940) which lays eggs on the backs of male and than the benefits. Why should an individual help Accepted 8 September 1999 Copyright © OIKOS 2000 ISSN 0030-1299 Printed in Ireland – all rights reserved 254 OIKOS 89:2 (2000) another if it suffers from helping? To date, no field Predators used in the experiments data exist regarding the predation risk faced by the golden egg bug or the potential costs associated with Pheidole pallidula is an extremely common ant species egg carrying. of the Mediterranean region, inhabiting dry, open habi- The present study was undertaken to examine pre- tats and borders of woods (Bernard 1968).Workers are dation by ants on the golden egg bug, and to evalu- small and dimorphic (minor worker 1.6–2.6 mm, major ate the costs of egg carrying. Ants have an important worker 3.3–4.9 mm, Bernard 1983) compared to (10 effect on the distribution and abundance of terrestrial mm) P. laciniata. However, workers are efficient preda- organisms (Wilson 1990). They detect moving objects tors quickly recruiting tens of workers to any edible while foraging and commonly use chemical cues to object (Szlep-Fessel 1970, Detrain 1990, Retana et al. locate prey (Ho¨lldobler and Wilson 1990). We focus 1992). They exhibit a bimodal diurnal rhythm with on predation of P. laciniata by Pheidole pallidula foraging activity interrupted during the hottest hours (Nylander) (Hymenoptera, Formicidae) and (Delalande 1985). Cataglyphis piliscapus (Forel) (Hymenoptera, Formi- By comparison, Cataglyphis piliscapus is both ecolog- cidae). These were the most common ant species in ically and geographically more restricted (Cagniant the study area and in habitats occupied by P. lacini- 1976, Lenoir et al. 1988). Cataglyphis species are indi- ata. P. pallidula individuals have also been noted to vidual foragers with C. piliscapus scavenging primarily attack eggs and bugs in the field (A. Kaitala, R. Ma- dead arthropods and collecting nectar (Retana et al. cias-Ordonez, M. Miettinen and R. L. Smith un- 1986). Their searching activity is strictly diurnal (Dela- publ.). lande 1985), coinciding with the activity patterns shown for P. laciniata. Materials and methods Experiments Natural history of the golden egg bug Our study was carried out in an abandoned vineyard located 3 km from Sant Climent Sescebes in Catalonia, P. laciniata is found in the Mediterranean region in north-eastern Spain. The principal ground cover is association with its primary host plants Paronychia Paronychia argentea, in which P. laciniata individuals sp. (Caryophyllaceae; Moulet 1995, Kaitala 1996). In are found in abundance (Kaitala 1996). the field individuals of both sexes carry eggs, but The experiments were carried out in open (32 cm males carry on average twice as many eggs as females diameter) circular enclosures. The inner and outer sur- (Kaitala 1996). Males receive more eggs than females face of the 4 cm high enclosures were covered by Fluon because they are often close to females due to copula- to prevent bugs from escaping and other invertebrates tion attempts and due to mate guarding after copula- from entering. The ants could easily escape via their tion (Kaitala and Miettinen 1997, Kaitala 1998). Egg tunnel system, and other insects could fly in. carrying does not increase male mating success We had three treatments: a) enclosures placed (Kaitala 1998). In populations where eggs are laid on around the entrance of Pheidole pallidula nests (or the backs they do not survive due to invertebrate tunnel entrance), b) enclosures placed on the entrance predation unless carried. In Catalonia, north-eastern of nests of Cataglyphis piliscapus and c) control enclo- Spain, the reproductive period starts in May, and sures placed randomly 2–5 m from the experimental during reproduction the bugs are most active in the enclosures. Control enclosures were placed on sites middle of the day (1100–1400 h). Although females where no ant activity was found before the experiment lay eggs for more than two months, they normally started and where no ant tunnels were found. Control lay only one or two eggs at a time (Kaitala and enclosures were treated with a small amount of insect Miettinen 1997). Eggs are glued firmly on the backs repellent (Merck Insect repellent 3535) to prevent ants of conspecifics, and they are very difficult to remove from digging an entrance. This was necessary because without causing damage to the host individual. Eggs in pre-experiments P. pallidula found bugs in control are large; one egg corresponds to about 4% of male enclosures within one or two days. body weight, and one male may carry up to 28 eggs Each enclosure contained the host plant P. argentea. on its back (Kaitala and Miettinen 1997). An egg-car- We marked bugs individually and counted the number rying individual does not provide any visible care to of eggs they carried. Ten bugs were released in each the eggs, and after hatching, the larvae leave the back enclosure (5 females, 5 males), and surviving bugs were of the carrying bug although egg shells remain on the recaptured after two days. If the wings were un- carrier’s back. Eggs removed from an individual in damaged, the tip of one flight wing was cut from P. the wild, survive and hatch well in the laboratory laciniata individuals with no or only a few eggs to (unpubl.). prevent escape by flying. This was done because in a OIKOS 89:2 (2000) 255 pre-experiment most bugs without eggs took off soon after being released in the enclosures. Eggs were mostly attached on the wings so that wings could not be cut if an individual carried eggs. However, bugs carrying several eggs are unable to fly (pers. obs.). Wings are small and transparent, and cutting the tip of one wing caused hardly any changes on their appearance. In some bugs the wings were already damaged, and cut- ting was unnecessary. This damage may be due to egg scraping (Kaitala 1999) or due to the fact that ants or other enemies had taken off the eggs and a piece of wing on which eggs were attached. The controls and P. pallidula experiments were car- Fig. 1. The loss of bugs from enclosures with workers of the ried out once on 27–29 May and once during 2–4 ant Pheidole pallidula (n=2×5 enclosures) and from controls June, 1997 with five replicates each time. The C.
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