Prediction of the Geographic Distribution of the Psyllid, Arytinnis hakani (Homoptera: Psyllidae), a Prospective Biological Control Agent of Genista monspessulana, Based on the Effect of Temperature on Development, Fecundity, and Survival Author(s): Lincoln Smith Source: Environmental Entomology, 43(5):1389-1398. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN14086 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. PHYSIOLOGICAL ECOLOGY Prediction of the Geographic Distribution of the Psyllid, Arytinnis hakani (Homoptera: Psyllidae), a Prospective Biological Control Agent of Genista monspessulana, Based on the Effect of Temperature on Development, Fecundity, and Survival LINCOLN SMITH1 Exotic and Invasive Weeds Research Unit, USDA Agricultural Research Service, 800 Buchanan Street, Albany, CA 94710 Environ. Entomol. 43(5): 1389Ð1398 (2014); DOI: http://dx.doi.org/10.1603/EN14086 ABSTRACT The psyllid, Arytinnis hakani (Loginova), is a prospective biological control agent of Genista monspessulana (French broom), an invasive shrub originating from western Europe. It is a multivoltine species that is not known to diapause. The insect is established in Australia, where it appears to cause heavy defoliation and mortality of the target weed, except at warm sunny sites. This suggests that bright light or high temperatures may hamper the agent. We measured the effect of temperature on development rate, survival, and fecundity of the psyllid to determine its suitable temperature range. Intrinsic rate of increase was highest near 22ЊC, and there was no population growth at the extremes of 5ЊC and 26ЊC. Net reproductive rate was highest at 16.5ЊC. Fecundity was highest at 22ЊC, and decreased to half at 16ЊC and at 27ЊC. Adult female longevity decreased with increasing temperature over the range studied. Nymphal survivorship was highest at 16ЊC and dropped to 0% at 5ЊC and 26ЊC. Eggs were able to complete development in 83 d at 5ЊC, but with only 20% survivorship versus 78Ð95% survivorship at higher temperatures. For populations with a stable age distribution, only 2Ð3% of the population is in the adult stage. Climate modeling using CLIMEX indicated that the geographic distribution of the psyllid is constrained by high temperature stress in Australia. The psyllid is predicted to be suitable in coastal California but not in the Sierra foothills. KEY WORDS population growth, demography, life history, temperature, climate matching Several psyllids are known to be important crop pests, ture on life history, can help us predict population and some have been used as biological control agents growth rates and model potential geographic distri- of invasive plants. For example, the Asian citrus psyl- butions (Van Klinken et al. 2003, Chiarelli et al. 2011, lid, Diaphorina citri Kuwayama (Homoptera: Psylli- Munyaneza et al. 2012, Myint et al. 2012). dae), transmits a pathogen that causes huanglongbing The psyllid, Arytinnis hakani (Loginova) is pro- (citrus greening disease; Grafton-Cardwell et al. spective biological control agent of French broom 2013), and the potato psyllid, Bactericera cockerelli (Genista monspessulana (L.) L.A.S. Johnson; Fabaceae: (Sˇulc), transmits a pathogen that causes zebra chip Genisteae) in North America (Sheppard and Thom- disease (Munyaneza 2012). Psyllid weed biological ann 2004, Cook and Smith 2014). A. hakani is native to control agents includeÑAphalara itadori Shinji for the western Mediterranean region, occurring from Japanese knotweed (Fallopia japonica (Houttuyn) Portugal to Italy in Europe, and from Morocco to Ronse Decraene), Arytainilla spartiophila (Fo¨rster) Algeria in North Africa. The psyllid is known to feed for Scotch broom (Cytisus scoparius (L.)), Boreiogly- on only G. monspessulana under natural Þeld condi- caspis melaleucae Moore for paper bark tree tions (Hodkinson and Hollis 1987, Sheppard and (Melaleuca quinquenervia (Cav.) Blake), and Heterop- Thomann 2004). The psyllid is multivoltine and not sylla spinulosa Muddiman, Hodkinson & Hollis for known to have any diapause. Eggs are attached to sensitive plant (Mimosa invisa Martius; Wilson and leaves and young stems by a pedicel. Nymphs progress Garcia 1922, Center et al. 2007, Syrett et al. 2007, Shaw through Þve instars as they feed on phloem from et al. 2009). Understanding the quantitative effects of leaves, stem branch tips, and ßowers. A. hakani was important environmental factors such as tempera- evaluated for introduction to Australia, but was dis- covered to already be established before a release permit was issued (Sheppard and Henry 2012). It now Mention of trade names or commercial products in this publication occurs in several Australian states, and high densities is solely for the purpose of providing speciÞc information and does not imply recommendation or endorsement by the USDA. of the psyllid are killing plants in many locations 1 Corresponding author, e-mail: [email protected]. (Sheppard et al. 2014). However, the psyllid does not 1390 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 5 appear to perform well in hot weather in Australia (Ϸ10 cm in height) in an incubator at constant tem- (A.W. Sheppard, personal communication). In south- perature and a photoperiod of 12:12 (L:D) h, illumi- ern France, the number of psyllids was reported to nated by four 20-watt ßuorescent bulbs (F20T12 day- decrease progressively during summer as tempera- light emitting 76 Ϯ 3 ␮EmϪ2 sϪ1 PAR tures rose, suggesting a decrease in oviposition or [photosynthetically active radiation]). Incubator immature survivorship; however, no data were pre- temperatures were set at 5, 10, 18, 22, 26, and 29ЊC. sented (Commonwealth ScientiÞc and Industrial Re- Adults were transferred daily to fresh cuttings to mea- search Organization [CSIRO] Entomology 2002). sure daily fecundity and adult survivorship (n ϭ 30, 23, Thus, high temperatures may be limiting the effec- 23, 23, and 20 at 10, 18, 22, 26, and 29ЊC, respectively). tiveness of this agent; however, no data are available Eggs changed from translucent white to opaque yel- quantifying the effect of temperature on demographic low after Ϸ3 d and were then counted because they life history characters. were easier to see. Eggs were monitored daily to re- The geographic distribution of some arthropods in- cord developmental time for eclosion and survivorship troduced as biological control agents of invasive (n ϭ 384, 280, 106, 102, 110, and 79 at 5, 10, 18, 22, 26, Њ weeds has been limited by climate (Byrne et al. 2004, and 29 C, respectively). Neonate L1 nymphs were Robertson et al. 2008). For example, the northern transferred to a young potted plant (7-Ð13 cm in distributions of Aceria chondrillae (Canestrini) and height) in groups of 5 per plant using a Þne pin at- Mecinus janthiniformis Toevski & Caldara are limited tached to an applicator stick (n ϭ 50, 80, 90, 49, 50, and by exposure to low temperatures in North America 98 at 5, 10, 18, 22, 26, and 29ЊC, respectively). Nymphs (De Clerck-Floate and Miller 2002; Milan et al. 2006). were monitored to measure development time and To select agents that are likely to have the most impact survivorship up to adult emergence. Each plant was on the target weed, it would be useful to be able to enclosed in a clear plastic drinking cup that had the assess the potential geographic distribution of a can- bottom cut out and the top screened with organdy, to didate before going through the long expensive pro- prevent escape of nymphs. Two cups were taped to- cess of meeting regulatory permitting requirements, gether in tandem to enclose tall plants. Plants were mass rearing, release, and establishment (McClay and watered as needed with tap water and no fertilizer was Balciunas 2005, Zalucki and Van Klinken 2006). One applied. method is to use existing data on the known distribu- Calculations and Statistical Analysis. Generalized tion of the agent in one region or continent to predict linear models (GLM) and RyanÐEinotÐGabrielÐ its distribution in another (Dhileepan et al. 2012, Mc- Welch multiple range tests (REGWQ) were used to Carren and Scott 2013). However, the geographic analyze the effect of temperature on the quantitative distribution of the target plant in the land of origin may response variables (longevity and fecundity; SAS In- be more constrained than in the adventive region stitute 2003). Response variables that could not be Þt (McFadyen 1991, Broennimann et al. 2014). In this by a linear or theoretical model were Þt by Bezier case, using only geographic data of the agentÕs distri- smoothing curves generated by Microsoft Excel (Figs.