Systematic & Applied Acarology 23(2): 401–403 (2018) ISSN 1362-1971 (print) http://doi.org/10.11158/saa.23.2.16 ISSN 2056-6069 (online)

Correspondence Responses of putrescentiae () to odour associated with its predator (Phytoseiidae)

XIAOYING WEI1 & ZHI-QIANG ZHANG1, 2 1 School of Biological Sciences, The University of Auckland, Auckland, New Zealand 2 Manaaki Whenua Landcare Research, 231 Morrin Road, Auckland, New Zealand; corresponding author email: [email protected]

In predator-prey interactions, the non-consumptive effects of predators have been studied much less than consumptive effects. Many such studies have focused on changes in the behaviour and ecology of the prey induced by the perception of predation risk. For example, the perception of predation risk can lead to a decrease in prey foraging rates (e.g. Lima, 1998; Brown and Kotler, 2004). Recent research on non-consumptive effects in showed that cues from predatory mites (Phytoseiidae) could influence the behaviour of prey mites, e.g. changes in oviposition sites or avoidance of risky sites with predator cues (Lemos et al. 2010; Dias et al. 2016). However, most research has focused on the impacts of predation risk on the behaviour of only phytophagous mites such as spider mites (Tetranychidae) (e.g. Grostal and Dicke 1998; Bowler et al. 2012) and gall mites (Eriophyidae) (Michalska 2016). Little is known about the non-consumptive effects of predatory mites on other kinds of mites such as the stored product Tyrophagus putrescentiae (Schrank) (Acaridae). Here, we test the behavioural response of T. putrescentiae to odour associated with one of its predators, Neoseiulus cucumeris (Oudmeans) (Phytoseiidae), using a choice test. N. cucumeris was selected in this study because (1) it is a widely available species and also a common predator of T. putrescentiae in stored products (Zhang 2003), and (2) it was recently used in our laboratory for other studies on predatory-prey interactions (e.g. Li and Zhang 2016; Patel and Zhang 2017a,b). This study is the first of a series of experiments on the non-consumptive effects of the presence of N. cucumeris on the behaviour and life history parameters of T. putrescentiae. The colonies of both mite species were purchased from Bioforce Limited in South Auckland and maintained in the laboratory (25°C, 80%RH, 14:10 h light:dark): N. cucumeris was fed T. putrescentiae which was reared on yeast (Li & Zhang 2016). The experimental arenas for choice tests were plexiglass slides (3×25×75 mm), each of which had a T-shaped tunnel (2.3 cm long and 1 cm high) linking three cells; the paired two cells were 0.8 cm in diameter, while the other cell was 0.5 cm in diameter. The bottom side of the slide was sealed by gluing on a fine 350-mesh cloth, and the top side was closed by a microscopic glass slide (3×25×75 mm) clamped with two metal clips. During a choice test, each individual mite (T. putrescentiae adult) was placed with a fine hair brush in the small cell and was observed whether it would go to Control or Test cell; both T and C cells contained yeast as food for test mites. There were three treatments: (1) T cell contained dead bodies of three T. putrescentiae that were frozen (–18 degrees, 24 h) with no prior contact with predators; (2) T cell contained dead bodies of three T. putrescentiae that were sucked dry by N. cucumeris; and (3) T cell contained the odour of N. cucumeris that was created by putting one adult predator mite in the T cell for 24 hours before the tests; the predator was removed before each test. There were 130 replicates per treatment. The numbers of T. putrescentiae in T or C cells were recorded at 1 h, 3 h, 6 h, and 24 h (Table 1); a small number of mites did not make a choice at the time of observation. These results were analyzed by chi-square test:

© Systematic & Applied Acarology Society 401 where o stands for observed and e for expected for mites choosing T cells (Table 1).

TABLE 1. Numbers of Tyrophagus putrescentiae adults choosing treatment (T) and Control (C) cells in choice tests after 1, 3, 6 and 24 h. Time Treatments numbers in T numbers in C chi-square df P value 1h Body of prey killed by freezing 44 61 2.752 1 0.097 Body of prey killed by predator 33 65 10.449 1 0.001 Odour of predator 33 67 11.56 1 0.0007 3h Body of prey killed by freezing 48 56 0.615 1 0.433 Body of prey killed by predator 39 58 3.721 1 0.054 Odour of predator 32 65 11.227 1 0.0008 6h Body of prey killed by freezing 42 56 2 1 0.157 Body of prey killed by predator 29 66 14.411 1 0.0001 Odour of predator 35 64 8.495 1 0.0036 24h Body of prey killed by freezing 47 48 0.012 1 0.918 Body of prey killed by predator 49 51 0.04 1 0.842 Odour of predator 55 52 0.084 1 0.772

Frozen dead bodies of T. putrescentiae did not have significant effects on the choice of T or C cells by T. putrescentiae. However, significantly fewer T. putrescentiae adults selected the treatment cells that contained dead bodies of T. putrescentiae killed by N. cucumeris or those with the odour left in the cell by N. cucumeris at 1 h, 3 h, and 6 h (but not 24 h). This indicates that T. putrescentiae can distinguish the cues of its predator and conspecifics killed by its predator. These results are consistent with many previous studies, which suggested that many can differentiate cues of their predators and other animals (e.g. Appelberg et al. 1993; Buchanan-Smith et al. 1993; Ward et al. 1996). This avoidance of their predators suggested these mites can perceive predation risk and this result is consistent with research on other mite prey species (Grostal & Dicke 1998; Utne & Bacchi 1997). Furthermore, with the passage of time, the influences of predator odour on the distribution of T. putrescentiae disappeared at 24 h, indicating the short-term nature of the effect of predator cues on prey in this study. Acknowledgement: To Kevin Chang (Statistical Consulting Centre, The University of Auckland, Auckland, New Zealand) for help with statistical analyses. To Guangyun Li and Jianfeng Liu (School of Biological Sciences, The University of Auckland, Auckland, New Zealand) for help in the laboratory. To Anne Austin (Manaaki Whenua Landcare Research, Palmerston North, New Zealand) and two reviewers (Systematic & Applied Acarology) for reviewing the manuscript and useful comments. Zhi-Qiang Zhang’s acarological research is supported by New Zealand Government core funding for Crown Research Institutes from the Ministry of Business, Innovation and Employment's Science and Innovation Group.

402 SYSTEMATIC & APPLIED ACAROLOGY VOL. 23 References

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Submitted: 24 Jan. 2018; accepted by Qing-Hai Fan: 14 Feb. 2018; published: 22 Feb. 2018

2018 WEI & ZHANG: RESPONSES OF TYROPHAGUS PUTRESCENTIAE TO ODOUR OF NEOSEIULUS CUCUMERIS 403