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Oviposition Habitat Selection in Response to Risk of Predation in Temporary Pools: Mode of Detection and Consistency Across Experimental Venue

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Oviposition Habitat Selection in Response to Risk of Predation in Temporary Pools: Mode of Detection and Consistency Across Experimental Venue Oecologia (2004) 138: 300–305 DOI 10.1007/s00442-003-1398-x BEHAVIOURAL ECOLOGY Leon Blaustein . Moshe Kiflawi . Avi Eitam . Marc Mangel . Joel E. Cohen Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue Received: 3 February 2003 / Accepted: 2 September 2003 / Published online: 27 November 2003 # Springer-Verlag 2003 Abstract Natural selection should favor females that mode of detection of the predator have important avoid ovipositing where risk of predation is high for implications for how to assess the true impact of predators their progeny. Despite the large consequences of such and for the use of commercially produced kairomones for oviposition behavior for individual fitness, population mosquito control. dynamics, and community structure, relatively few studies have tested for this behavior. Moreover, these studies have Keywords Culiseta longiareolata . Chironomus riparius . rarely assessed the mode of detection of predators, Kairomone . Notonecta maculata . Temporary ponds compared responses in prey species that vary in vulner- ability to predators, or tested for the behavior in natural habitats. In an outdoor artificial pool experiment, we tested Introduction the oviposition responses of two dipteran species, Culiseta longiareolata (mosquito) and Chironomus riparius Numerous studies have documented a variety of induced (midge), to the hemipteran predator, Notonecta maculata. responses by prey to risk of predation in aquatic systems Both dipteran species have similar life history character- (reviews in Chivers and Smith 1998; Kats and Dill 1998; istics, but Culiseta longiareolata larvae are highly Dicke and Grostal 2001). Only a surprisingly small vulnerable to predation by Notonecta, while Chironomus fraction of these has considered oviposition decisions riparius larvae are not. As their vulnerabilities would based on risk of predation to progeny (reviews in suggest, Culiseta longiareolata, but not Chironomus Blaustein 1999; Skelly 2001). Yet, such oviposition riparius, strongly avoided ovipositing in pools containing behavior may strongly affect individual fitness, population Notonecta. An experiment in natural rock pools assessing dynamics, and community structure (Blaustein 1999; oviposition by Culiseta longiareolata in response to Spencer et al. 2002). When oviposition habitat selection Notonecta maculata yielded an oviposition pattern highly (OHS) in response to risk of predation has been consistent with that of the artificial pool experiment. We documented, chemical detection of the predator has often also demonstrated that the cue for oviposition avoidance been suggested as the likely cue (McCall 2002), but by Culiseta longiareolata was a predator-released chem- studies designed to test for this adequately are rare [aquatic ical: Notonecta water (without Notonecta replenishment) systems: Berendonck (1999); Angelon and Petranka repelled oviposition for 8 days. Oviposition avoidance and (2002); terrestrial systems: Grostal and Dicke (1999)]. Moreover, in the limited studies assessing this oviposition . L. Blaustein (*) M. Kiflawi . A. Eitam behavior, potential prey species that are predicted to Community Ecology Laboratory, Institute of Evolution, exhibit OHS are usually tested while “unlikely” species, University of Haifa, 31905 Haifa, Israel with rare exceptions (Berendonck and Bonsall 2002), are e-mail: [email protected] ignored. Tel.: +972-4-8240736 Blaustein (1999) suggested that evolution of OHS in Fax: +972-4-8246554 response to risk of predation is more likely when: M. Mangel 1. Progeny are highly vulnerable to the predator; Applied Mathematics and Statistics, University of California, 2. Prey have few lifetime reproductive events; Santa Cruz, CA 95064, USA 3. Eggs for each reproductive cycle are laid together as a J. E. Cohen single clutch and are not spread across multiple sites; Laboratory of Populations, Rockefeller and Columbia 4. Predator density is highly heterogeneous among patch- Universities, es; New York, NY 10021, USA 301 5. Predator distributions among patches are highly fixed opportunities and it lays all its eggs in a cluster (Armitage from the prey oviposition event until the prey progeny et al. 1995). However, in contrast to Culiseta long- can either leave the patch or become large enough to be iareolata, Chironomus larvae have low vulnerability to invulnerable to predation. predation by N. maculata (Blaustein 1998). Consequently, we predicted that Chironomus riparius would not exhibit These criteria, particularly the fifth one, are more OHS in response to N. maculata. common in predator-prey systems of temporary pools than In previous studies comparing equal numbers of pools in terrestrial habitats (Blaustein 1999). All stages of containing N. maculata and not containing N. maculata, microinvertebrate predators such as flatworms and cyclo- approximately 90% of the Culiseta egg rafts were poid copepods, and pre-metamorphic stages of insect observed in N. maculata-free pools (Blaustein et al. predators and urodeles are confined to the pool from 1995; Blaustein 1998; Spencer et al. 2002; Kiflawi et al. which they hatched or were born. 2003a). While OHS is the likely explanation of this Almost all experimental studies assessing OHS in distribution of egg rafts, these studies were not designed to response to risk of predation in pool habitats have used eliminate alternative explanations, i.e., predation on either artificial pools as their experimental venue (e.g., Chesson egg rafts or females alighting on the water to oviposit 1984; Resetarits and Wilbur 1989; Hopey and Petranka (Chesson 1984). The present study was designed both to 1994; Blaustein et al. 1995; Resetarits 2001; Binckley and differentiate between the OHS hypothesis and these Resetarits 2002), with only a few exceptions using natural alternative hypotheses, and to discriminate between pools (Laurila and Aho 1997; Speiler and Linsenmair chemical detection and other cues for detecting the 1997). The reason for using artificial pools over natural predator. We show that OHS occurs as predicted relative ones is clear: ease of true and adequate replication (Wilbur to vulnerability to predation by the backswimmer, and that 1997; Morin 1998; Blaustein and Schwartz 2001; Skelly detection of the predator is via chemical cue. We also and Kiesecker 2001). However, some studies assessing show that the pattern is consistent in two experimental ecological interactions have shown that the outcome may venues: outdoor artificial and natural pools. differ in natural versus artificial pools. For example, Marsh and Borrell (2001) showed that, in an artificial pool experiment, the tungara frog strongly avoided ovipositing Materials and methods in pools containing conspecific egg masses and tadpoles, but in a natural pool experiment, no such pattern was Artificial pool experiment detected. Here, we compare the oviposition responses of two We conducted an artificial pool experiment at Hai Bar Nature Reserve, Mt Carmel, northeastern Israel. Fourteen plastic tubs dipteran prey species, the mosquito Culiseta longiareolata (0.6×0.4 m, 0.14 m depth; ~33.6 l) were placed in a 2×7 grid (inter- Macquart (Diptera: Culicidae) and the midge Chironomus pool distance ~0.4 m) under a 90% shade net suspended at a height of 2 m. On 9 April 2000 we filled the tubs with tap water and added riparius Meigen (Diptera: Chironomidae), to risk of 3 predation by a predatory backswimmer, Notonecta 14 cm of fish food pellets for nutrients. Water volume was maintained at ~13 cm depth (~31 l) with aged tap water. Seven pools maculata Fabricius (Hemiptera: Notonectidae), and the were randomly assigned as control (no N. maculata) pools and mode of predator detection by the dipteran adults, if OHS seven as predator (N. maculata) pools. A cage, made from a 2 l occurs. We also experimentally determine if oviposition plastic bottle containing three 50 cm2 screen windows (mesh size patterns exhibited in artificial pools are consistent with 1 mm), was placed into, and removed from, each pool as described below. The cages in predator pools contained five N. maculata patterns in natural pools. The predator and prey species are nymphs (instars IV–V) each while cages in control pools did not common in temporary pools of Israel (e.g., Ward and have N. maculata. Blaustein 1994; Blaustein and Margalit 1995; Blaustein The experiment consisted of three phases. During the first phase, 1998). Notonecta maculata nymphal instars are largely, if we placed the cages into the pools each morning (~08:00), removed not completely, confined to the pool in which their eggs them before sunset, and returned them the following morning. Because Culiseta longiareolata females oviposit at night, Culiseta were oviposited. Adult N. maculata can remain in the longiareolata females searching for an oviposition site would thus same pool or disperse to other pools (Briers and Warren not be exposed to the N. maculata themselves, but only to any 2000). Culiseta longiareolata meets all of the criteria that possible chemical cues. Each morning, beginning when Culiseta Blaustein (1999) suggested for the likelihood of OHS in longiareolata began ovipositing into these pools (11 April), we counted and removed mosquito egg rafts and chironomid egg response to N. maculata. This mosquito lays all its eggs strings. During this period (9 nights), we saved five randomly together as an egg raft. Immature development time (~2– selected
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