Is it enemy‐free space? The evidence for terrestrial insects and freshwater arthropods

Abstract

Abstract. Enemy‐free space (EFS) was defined by Jeffries & Lawton (1984) as ‘ways of living that reduce or eliminate a species’ vulnerability to one or more species of natural enemies’. EFS has emerged in the literature as a significant niche‐moulding factor. However, the lack of consistency among the empirical studies as to how EFS should be defined, and what hypotheses should be tested in order to evaluate its relative importance, prompted us to review the literature and to propose a working definition that results in a general set of testable hypotheses. To test the relative importance of EFS in structuring the communities of organisms, we propose a set of three falsifiable null hypotheses that must be tested sequentially and rejected. Ho1: The fitness of the organism in an original habit (e.g. on an original host plant) in the presence of natural enemies is equal to the fitness of the organism in that habit in the absence of natural enemies. Acceptance of the alternative hypothesis that the fitness of the organism in the presence of natural enemies is less than in the absence of natural enemies is necessary to demonstrate the importance of natural enemies. Ho2: The fitness of the organism in an alternative habit with natural enemies is equal to the fitness of the organism in the original habit with natural enemies. Acceptance of the alternative hypothesis that the fitness of the organism in the alternative habit with natural enemies is greater than that in the original habit with natural enemies is necessary to demonstrate that the alternative habit provides EFS. Ho3: The fitness of the organism in an alternative habit without natural enemies equals the fitness of the organism in the original habit without natural enemies. Acceptance of the alternative hypothesis that the fitness of the organism in an alternative habit without natural enemies is less than in the original habit without natural enemies is necessary to demonstrate the relative importance of EFS compared with other co‐occurring niche‐moulding factors such as competition or host nutritional quality. We searched the literature and evaluated fifty‐three references (nineteen references to seventeen different terrestrial systems and thirty‐four references to twenty‐four different freshwater systems) to test our hypotheses. Of the forty‐one systems examined, nineteen (46%) tested only for differences in vulnerability of the prey or host species between EFS and non‐EFS options (our Ho2); sixteen (39%) tested for the importance of natural enemies and the effectiveness of the alternative habit in providing EFS (our Ho1 and Ho2); and only ten systems (24%) tested for Ho1, Ho2 and the relative importance of EFS in the system as measured by fitness (our Ho3). Of the systems that tested for EFS, sixteen of nineteen (84%), thirteen of sixteen (81%) and seven of ten (70%) showed evidence in support of the existence of EFS according to hypothesis Ho2 only, hypotheses Ho1 and Ho2, and our three working hypotheses, respectively. These results indicate that very few studies have actually tested for the existence of EFS. Nevertheless, results from this limited number of natural systems suggest that EFS may be important in moulding the niches of arthropods. Because of the large number of claims for EFS in systems where none of the basic hypotheses were investigated, we suggest that authors test for EFS experimentally, be judicious in selecting articles to cite in support of EFS, and exert care in attributing it as a selective force in the evolution of arthropods in specific systems.

Dietary specialization influences the efficacy of larval tortoise beetle shield defenses

“…There is scant evidence that specialists gain enemyfree space by incorporating host-derived compounds into predator defenses or by other means that increase their resistance to attack (Berdegue et al 1996;Stamp 2001). Several studies showed reduced vulnerability of specialist caterpillars reared on or collected from different host plants (Bernays 1988(Bernays , 1989Bernays and Cornelius 1989;Dyer and Floyd 1993).…”

Detection of refuge from enemies through phenological mismatching in multitrophic interactions requires season-wide estimation of host abundance

“…Dozens of examples of studies involving enemy-free space can be found in the literature (Ohsaki and Sato 1994;Berdegue et al 1996;Scheirs and De Bruyn 2002;Murphy 2004;Heard et al 2006). Amongst the mechanisms generating enemy-free space, asynchrony in seasonal distribution of natural enemies and their hosts (Feder 1995) forms a prominent example.…”

“…Barbarea has also been found to be a less profitable host plant compared to the alternative host plants (in agreement with condition three ;Nielsen 1999;de Jong and Nielsen 2000); this was indeed the incentive for the present study (see above). In this research the remaining condition formulated by Berdegue et al (1996) was addressed, namely whether mortality caused by natural enemies is lower on Barbarea than on Sinapis, and whether this is related to the difference in phenology of the different host plants. We explicitly studied the possibility of enemy-free space by not only determining the percentage parasitism of host samples collected throughout the season, but by also estimating the host population dynamics over the period of sampling to enable the calculation of a season-wide risk of parasitism of flea beetle larvae using different host plants as food.…”

“…To test for enemy-free space, three conditions as formulated by Berdegue et al (1996) should be addressed. The first condition tests the importance of natural enemies in the system.…”

Presence of the fire ant Solenopsis invicta (Westwood) (Hymenoptera: Formicidae) stimulates burrowing behavior by larvae of the sandfly Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae)

“…The importance of refuges in predator-prey relationships is that they provide 'enemy-free space' and thus prevent over-exploitation of prey populations through predation (Berdegue et al 1996). Moreover, the production of allomones in defense may secondarily act as kairomones that attract specialist natural enemies (Corbet1968, De Baur & Yeargan 1994).…”