Temperature-dependent development of glabratus (Coleoptera: : Scolytnae) Gurpreet S. Brar1,*, John L. Capinera2, Paul E. Kendra3, Jason A. Smith4, and Jorge E. Peña5

Abstract Redbay ambrosia , Eichho Coleoptera: Curculionidae: Scolytnae, is a nonnatve that transmits the pathogenic Rafaelea lauricola T.C. Harr., Fraedrich Aghayeva phiostomatales: phiostomataceae, hich causes laurel ilt disease in of the family . Laurel ilt is present in the commercial Persea americana Mill.; Laurales: Lauraceae groing areas of Florida and poses a potental threat to the avocado industries of California and Meico. The life cycle of X. glabratus as studied in avocado logs at 16, 20, 24, 28, and 32 C. Xyleborus glabratus successfully completed its life cycle at 24, 28, and 32 C, ith the greatest ovipositon and development rate at 28 C. Development of the egg and pupal stages as studied at 12, 16, 18, 20, 24, 28, 32, and 36 C. ne linear and nonlinear developmental models ere used to estmate the temperature-dependent development of both stages. The linear model estmated the loer threshold temperatures for egg and pupal development to be 13.8 C and 11.1 C, respectvely, and the degree-days DD for egg and pupal development to be 55.1 DD and 68.2 DD, respectvely. The Brier-2, Ratosy, Logan, and polynomial models gave the best estmates for the temperature-dependent development of the egg stages, hereas the Brier-1, Logan, and polynomial models gave the best estmates of temperature-dependent development of the pupal stages. ur results suggested that the optmal temperature for development of X. glabratus as around 28 C, and that temperature ill play an important role in the spread and successful establishment of X. glabratus.

ey ords: avocado; redbay, temperature; development models

Resumen El escarabajo ambrosia del laurel rojo, Xyleborus glabratus Eichho Coleoptera: Curculionidae: Scolytnae es una plaga no natva y el vector del hongo patgeno Rafaelea lauricola T.C. Harr., Fraedrich Aghayeva, ue causa la enfermedad de la marchite del laurel en los rboles de la familia Lauraceae. La marchite del laurel est presente en reas de la Florida donde se siembra el aguacate comercial Persea americana Mill y representa una amenaa potencial para las industrias de aguacate en California y Mico. Se estudi el ciclo de vida de X. glabratus en troncos de aguacate a los 16, 20, 24, 28 y 32 C. Xyleborus glabratus complet con ito su ciclo de vida a los 24, 28 y 32 C, con la tasa de oviposicin y desarrollo ms alto a los 28 C. Se estudi el desarrollo del huevo y a los 12, 16, 18, 20, 24, 28, 32 y 36 C. Un modelo lineal y modelos no lineales de desarrollo fueron utliados para modelar el desarrollo del huevo y pupa dependiente de la temperatura. El modelo lineal result en un estmado del umbral de la temperatura inferior para desarrollo de huevos y de 13.8 C y 11.1 C, respectvamente, y del nmero de grados-da GD para el desa- rrollo de huevos y pupas a 55.1 GD y 68.2 GD, respectvamente. Los modelos Brier-2, Ratosy, Logan y polinomiales dio las meores estmaciones para el desarrollo del estadio de huevo dependiente de la temperatura, mientras ue los modelos Brier-1, Logan y polinomiales dieron las meores estmaciones para el desarrollo del estadio de pupa dependiente de la temperatura. Nuestros resultados sugieren ue la temperatura ptma para el desarrollo de X. glabratus es alrededor de 28 C, y ue la temperatura va a ugar un papel importante en la propagacin y establecimiento eitoso de X. glabratus.

Palabras Clave: aguacate; laurel roo; temperatura; modelos de desarrollo

The eotc redbay , Xyleborus glabratus Eichho the laurel ilt pathogen has been detected in the folloing Lauraceae Coleoptera: Curculionidae: Scolytnae has become a serious pest of species: redbay L. Spreng., avocado Persea ameri- trees of the family Lauraceae in the United States. The beetle is natve cana Mill., sampbay Persea palustris Raf. Sarg., silbay Persea to Southeast Asia and as introduced accidentally in the southeastern humilis Nash, sassafras Nu. Nees, northern United States around 2002 Haac 2003; Rabaglia et al. 2008; Pea et spicebush Lindera benzoin L. Blume, pondspice Litsea aestvalis [L.] al. 2012. The redbay ambrosia beetle transmits the fungus Rafaelea Fernald, pondberry Lindera melissifolia alter Blume, and cam- lauricola T.C. Harr., Fraedrich Aghayeva phiostomatales: phiosto- phor Cinnamomum camphora L. . Presl. It sometmes causes mataceae, Fraedrich et al. 2008; Hanula et al. 2008 that causes lau- mortality of 0 of infested trees Fraedrich et al. 2008; Mayeld et al. rel ilt, a lethal vascular disease. Since the introducton of the beetle, 2008; Smith et al. 200a, b; Hughes et al. 2013. Eperimental inocula-

1Everglades Research and Educaton Center, University of Florida, IFAS, 3200 E Palm Beach Rd, Belle Glade, FL 33430, USA 2Entomology and Nematology Department, University of Florida, IFAS, Gainesville, FL 32611, USA 3Subtropical Hortculture Research Staton, USDA-ARS, Miami, FL 33158, USA 4School of Forest Resources and Conservaton, University of Florida, Gainesville, FL 32611, USA 5Tropical Research and Educaton Center, University of Florida, IFAS, Homestead, FL 33031, USA *Corresponding author; E-mail: [email protected]

856 2015 — Florida Entomologist — Volume 98, No. 3 Brar et al.: Temperature-dependent development of the redbay ambrosia beetle 85 tons ith R. lauricola indicate that California bay laurel Umbellularia rial Forest Alachua County, rday-Sisher Biological Staton Put- californica Hoo Arn. Nu. and Gulf licaria Licaria triandra S. nam County, and Hammoc Dunes Club Golf Course, Palm Bay Bre- osterm. also are susceptble Fraedrich 2008; Ploet onol 2013. vard County. Infested logs ere collected, and a beetle colony as Identcal rates of development of X. glabratus ere observed in avo- maintained at the University of Florida, Entomology and Nematology cado, redbay, and sampbay logs held at 25 2 C, ith teneral adult Department, Gainesville Alachua County, Florida, USA, by methods stages encountered approimately 1 mo aer gallery initaton Brar previously reported Brar et al. 2013. et al. 2013. The emissions of -cubebene, -copaene, -humulene, and calamenene from host trees ere correlated ith aracton of REARING F X. GLABRATUS FR DEELPMENTAL STAGES adult to the host trees endra et al. 2011, 2014. Laurel ilt currently is present in commercial avocado groves in southern Florida Avocado Booth logs measuring 4.5 to 6.5 cm in diameter and 8 FDACS 2012 and has been the subect of recent revies endra et to 10 cm in length from healthy trees ithout beetle infestaton ere al. 2013; Ploet et al. 2013. procured from the University of Florida, Tropical Research and Educa- Since its introducton, the redbay ambrosia beetle has been report- ton Center, Homestead Miami Dade County, Florida, USA. Logs ere ed in North Carolina, South Carolina, Georgia, Florida, Alabama, and soaed in tap ater for 48 h, removed, and individually placed in 46 Mississippi, USA, and its range has epanded more uicly than pre- mL clear plastc containers American Plastcs, Gainesville, Florida, dicted by och Smith 2008. Beetle populaton dynamics studies in USA. Each container as covered ith Planton neng 150 microns, South Carolina and Georgia, USA, have shon that adult beetles ere Biouip, Rancho Domingue, California, USA. To eep the logs moist, actve throughout the year, ith greater fight actvity in Sep compared appro. 100 mL of ater ere maintained in each container through- ith an and Feb Hanula et al. 2008, 2011. In Alachua County, Florida, out the eperiment. Tenty scleroted female adult beetles ere USA, strong actvity of the beetles as recorded in Apr 2010, ct 2010, placed directly on the bar of each log and ere alloed to bore. Logs and Mar 2011, hereas lile actvity as recorded in Nov 2010, Dec ere ept in an incubator Precision® illuminated incubator, Precision 2010, and an 2011 Brar et al. 2012. This suggests that the beetles are Scientc Inc., Chicago, Illinois, USA at 25 2 C in complete darness. more actve in the summer months than in colder months in northern The number of logs infested on a given day as dependent on the Florida. ariaton in temperature, along ith other climatc variables, number of adult females available. Infested logs ere divided into 2 might play an important role in the populaton dynamics of this spe- sets, one for collecton of eggs and the other for collecton of pupae. cies Brar et al. 2012. Given the potental impact of the beetlefungus Based on data previously obtained regarding the life cycle of X. glabra- comple on the avocado industry of Florida and California, USA, and its tus on avocado Brar et al. 2013, the logs ere split and galleries care- potental threat to other lauraceous plants throughout North, Central, fully opened ith a hand pruner Fisars compound anvil hand pruner, and South America Gramling et al. 2010; Pea et al. 2012, it is desir- Loes, Gainesville, Florida, USA on the 10th to 13th day aer gallery able to develop phenological and populaton dynamics models to help initaton, and eggs ere carefully etracted ith sterilied needles. In predict pest infestatons, and to initate control measures. lie manner, the logs ere split, galleries carefully opened on the 24th Climate limits the distributon of pests, ith temperature to 26th day aer gallery initaton, and pupae ere etracted. being one of the abiotc factors that play a maor role. noledge of insect development in relaton to temperature is critcal in order to un- derstand insect populaton dynamics, but noledge of temperature DEELPMENT F EGG AND PUPAL STAGES AT CNSTANT relatons is also essental to create phenological predictve models. TEMPERATURES During the last fe decades, various mathematcal models have been The duraton of development from egg to larval stage and from used to model temperature-dependent development of . These pupal to adult stage as studied at constant temperatures. Eggs e- models range from simple linear models Campbell et al. 14; Roy et tracted from avocado logs ere placed in Petri dishes 50 mm, BD al. 2002 that can predict the loer developmental threshold tempera- Falcon, Franlin Laes, Ne ersey, USA lined ith moist paper toel. ture ithin limited ranges of temperature, to nonlinear mathematcal Petri dishes ere placed in Florida Reach-In incubators aler et al. models Logan et al. 16; Taylor 181; Ratosy et al. 183; Lamb 13 held at constant temperatures of 12, 16, 20, 24, 28, 32, and 36 C at al. 184; Lactn et al. 15; Briere et al.1 that can describe tem- 0.1 C and ept under constant darness. For each temperature, the perature-dependent development over ider ranges of temperatures. numbers of larvae that hatched ere recorded daily. Numbers of eggs Nonlinear models have been compared to nd the model that reliably used for each temperature study ere dependent on the numbers predicts development close to actually observed values based on com- available aer spling the logs. The number of eggs placed at each 2 monly used criteria such as higher r coecient of determinaton temperature ranged from 20 to 60. Pupae etracted from avocado logs and loer RSS residual sum of suares and AIC Aaie informaton ere placed in Petri dishes folloing the same method used for eggs. algama aluci 200b; Aghdam et al. 200; Sandhu et al. 2010, Numbers of pupae placed at each temperature treatment ranged from 2013. The obectves of this study ere to 1 evaluate temperature- 20 to 45. The number of days reuired for the development of egg to dependent development of the egg and pupal stages of X. glabratus, the 1st instar and from the pupal to the adult stage for all temperature 2 develop a valid model based on various linear and nonlinear models, treatments as recorded daily. Paper toels ere ept moist to pre- and 3 study the life cycle and temperature-dependent development of vent desiccaton of insects. The study as conducted beteen Mar and X. glabratus in avocado logs placed at dierent constant temperatures. un 2012. Temperature-dependent development of the various larval instars as not studied due to lac of an adeuate artcial medium on hich to rear larvae. Materials and Methods LIFE CCLE AND DEELPMENT F X. GLABRATUS IN ACA BEETLE SURCE D LGS AT CNSTANT TEMPERATURES Redbay and sampbay trees ith high infestatons of X. glabratus The life cycle and development of X. glabratus in avocado logs ere ere scouted at 3 locatons in Florida, USA, i.e., Austn Cary Memo- studied at 5 constant temperatures 16, 20, 24, 28, and 32 C dur- 858 2015 — Florida Entomologist — Volume 98, No. 3

2 2 2 2 2 ing Sept 2011 to May 2012. Avocado Booth logs of 4.5 to 6.5 cm Topt = [2mTm m 1 T0 4m Tm m 1 T0 4m TmT0 4m + 2 1 diameter ere cut from healthy trees ithout any beetle infestaton from the University of Florida, Tropical Research and Educaton Center, The m is the empirical constant ith value 2 for the Briere model Homestead Miami Dade County, Florida, USA. The logs ere cut to 8 Briere Pracros 18. In the Lactn and Logan models, Topt can be to 10 cm length, soaed in tap ater for 48 h, and then placed in a 46 estmated as the parameter value for hich the rst derivatve euals mL clear plastc container American Plastcs, Gainesville, Florida, USA. ero. In the Taylor model, Topt can directly be estmated from the model Depending on the availability of beetles, 5 to 20 scleroted adult fe- Table 1. The value of K can be estmated by linear regression Camp- male beetles ere placed on each log and alloed to bore for 24 h at 25 bell et al. 14. Criteria used to compare performance of nonlinear 2 2 C. Each container as covered ith Planton neng 150 microns, mathematcal models ere 1 coecient of determinaton r , here- Biouip, Rancho Domingue, California, USA. Aer 24 h of infestaton, in the higher value indicates a beer t of the model, and 2 residual infested logs ere placed in Florida Reach-In incubators aler et al. sum of suares RSS, herein the loer value indicates a beer t of 13 held at 5 constant temperatures 16, 20, 24, 28, and 32 C the model Aghdam et al. 200. A third additonal criterion, the Aaie 0.1 C under complete darness. For each temperature treatment, 60 informaton criterion AIC as used to compare nonlinear models. The logs ere infested and studied for 40 d. For each temperature treat- model that has the loer AIC value has a beer t hen comparing ment, every other day, 3 logs or 3 replicates ere randomly removed models. AIC as calculated by Euaton 2. from the incubators, and for each log, 5 actve galleries ith signs of fresh frass ere mared ith a permanent marer Sharpie pen. The AIC n lnSSE / n 2p 2 logs ere split to epose the mared galleries, and galleries ere fur- here n is the sample sie, p is the number of parameters, and SSE is ther dissected to record the number of insects at each developmental the sum of the suared errors. stage. The hole study as repeated tice. Data for dierent eperiments ere tested ith Shapiroil normality tests Shapiro il 165 to ensure that the assumptons MATHEMATICAL MDELS AND STATISTICAL ANALSES of homogeneity of variance and normality ere met before the data ere analyed. To determine dierences beteen the duraton of de- The development rate of eggs and pupal stages as regressed velopment from egg to larval stage and from pupal to adult stage at against temperature in linear and nonlinear models. Seven nonlinear dierent constant temperatures, e subected the data to separate models Table 1 used to describe temperature-dependent develop- 1-ay analysis of variance ANA and Tueyramer tests, by Proc ment of insects—such as Halyomorpha halys Stal Hemiptera: Pen- GLM in SAS SAS 2003. Linear regression SAS as used to model the tatomidae Nielsen et al. 2008, Cydia pomonella L. Lepidoptera: rate of development for each stage at 16, 20, 24, and 28 C. The linear Tortricidae Aghdam et al. 200, Plutella xylostella L. Lepidoptera: model y = a + bx Campbell et al. 14 as used to estmate the loer Plutellidae Goliadeh et al. 200, and Elasmopalpus lignosellus developmental threshold temperature Tmin a / b, and thermal con- eller Lepidoptera: Pyralidae Sandhu et al. 2010, 2013ere stant K = 1 / b. Seven nonlinear models Table 1 ere used to model used to describe temperature-dependent development of the egg and temperature-dependent development of the egg and pupal stages. pupal stages of X. glabratus. The estmated parameters ere T0 the The nonlinear models ere ed ith the Maruardt algorithm Mar- temperature at, or belo, hich no measurable development as vis- uardt 163 in SAS soare. The dierences in tme to occurrence of ible; also called loer development threshold Hoell Neven 2000; dierent development stages aer inital infestaton of avocado logs at

Sandhu et al. 2010, Tm upper development threshold, temperature at, dierent constant temperatures ere analyed by conductng ANA or above, hich no visible development taes place ontodimas et in SAS. Tueyramer tests ere conducted to ascertain dierences al. 2004; Sandhu et al. 2010, Topt temperature at hich highest rate of in duraton of developmental stages of the beetle in logs at constant development taes place Briere Pracros 18; Sandhu et al. 2010, temperatures using SAS. and K thermal constant; the number of degree-days reuired by an immature stage to complete its development Campbell et al. 14;

Aghdam et al. 200. The value of T0 can be estmated from a linear Results model and from 3 nonlinear models Briere-1, Briere-2, and Ratosy and Taylor. T can be estmated by nonlinear models Briere-1, Bri- m EGG DEELPMENT ere-2, Lactn, and Logan. Topt can be calculated ith the Taylor, Bri- ere-1, Briere-2, and Lactn and Logan models. In the Briere-1 and Bri- Temperature had a signicant eect on egg development F = ere-2 models, Topt can be calculated by Euaton 1. 192.3; df = 5, 188; P 0.0001 Table 2. No development as observed

Table 1. Mathematcal euatons of nonlinear developmental models tested to describe the relatonship beteen temperature and development of egg and pupal stages of Xyleborus glabratus.

Developmental model Mathematcal euaton References

Briere-1 model r = aTT T0 srtTm T Briere et al. 1 1 d Briere-2 model r = aTT T0 Tm T ] Briere et al. 1 T T T Logan model rT e e m m Logan et al. 16 T T T Lactn model rT e e m m + l Lactn et al. 15 Polynomial model r = aT4 + bT3 + cT2 + dT e Lamb et al. 184 2 Taylor model r = Rm ep0.5T Topt T0] } Taylor 181

Ratosy model r = bT T0 1 epcT Tm Ratosy et al. 183

r rate of development; T treatment temperature ; T0 loer temperature threshold; Tm lethal maimum temperature; Topt optmum temperature ; r development rate at optmal temperature ; D no. of degrees above the base temperature over hich thermal inhibiton becomes predominant; m empirical constant; l empirical constant hich forces the curve to intercept the y-ais at a value belo ero; Rm maimum development rate; a, b, c, d, e empirical constant. Brar et al.: Temperature-dependent development of the redbay ambrosia beetle 85 Table 2. Mean SE number of days reuired for development of Xyleborus Table 4. Nonlinear regression parameters, ed coecients, and evaluaton in- glabratus eggs and pupae at constant temperatures. dices of nonlinear models tested for temperature-dependent development of eggs and pupae of Xyleborus glabratus. Developmental period in days Model Parameter Eggs Pupae Eggs Pupae Briere-1 a104 1.64 2.10 Temperature C N Mean SE N Mean SE T0 11.3 11.3 T 36.4 33.4 16 30 21.1 0.5 a 35 12. 0.51 a m T 31.5 29.5 20 43 .5 0.21 b 34 .1 0.31 b opt 2 24 36 6.6 0.30 c 26 5.8 0.20 c r 0.86 0.91 28 41 3. 0.1 d 26 4.3 0.22 d RSS 0.8114 0.351 32 24 .3 0.51 c 28 6.4 0.26 c AIC 88.4 02.34 36 20 10. 0.5 b Briere-2 a104 0.06 2.0 d 0.9968 45.0 Means folloed by the same leer are not signicantly dierent based on the Tuey ramer test for dierence of means P 0.05. N Number of eggs or pupae that developed T0 14.4 8.9 to the net stage in the life cycle. Tm 3. 32.0

Topt 32.3 2.1 2 in eggs held at 12 C. Successful progression from egg to the 1st instar r 0.88 0.88 occurred from 16 to 36 C, ith the fastest development rate observed RSS 0.446 0.545 AIC 8.83 834.3 at 28 C Table 2. Mean development tme for eggs ranged from 21.1 0.5 d at 16 C to 10. 0.5 d at 36 C Table 2. A linear regression Lactn r 0.0659 0.2251 model of temperatures ranging from 16 to 28 C ith development D 13.31 4.44 rate yielded a loer temperature threshold of 13.8 C, reuiring 52.1 Tm 43.1 34.3 DD for beetles to develop from egg to the larval stage Table 3. Topt 29.8 29.9 The model evaluaton parameters, ed coecients, and evaluaton l 0.58 0.0842 2 criteria indices for nonlinear models tested for temperature-depen- r 0.53 0.3410 dent development of egg to larval stages are presented in Table 4. The RSS 0.51 0.530 estmated optmum temperature for development of egg to larval stage AIC 86.36 836.85 ranged beteen 32.3 C Briere-2 model and 2. C Taylor model. In Logan r 0.1561 0.19 general, all the models gave a good t ith r2 values above 0.85, ecept D 6.41 5.04 2 for the modied Lactn model, here the r value as 0.53. The Briere-2, Tm 3.0 33. Ratosy, polynomial, and Logan models gave beer ts than other Topt 28. 28. 2 models based on a greater r2 value and smaller RSS and AIC values. The r 0.92 0.93 Taylor model gave a good t based on the greater r2 value and smaller RSS RSS 0.848 0.31 and AIC values, but its estmated loer development thresholds ere AIC 0.16 1.5

less than the observed values. The Logan model provided estmates of Taylor Rm 0.2455 0.222

Tma 3.0 C and Topt 28. C. The Ratosy and Briere-2 models pro- Topt 2. 2.4 T 5.8 .2 vided estmates of T0 14.4 C that ere closer to the observed values. 0 r2 0.89 0.91 PUPAL DEELPMENT RSS 0.628 0.322 Temperature had a signicant eect on the development of the AIC 805.04 83.84 pupal stage F .5; df 4, 144; P 0.0001 Table 2. No pupal de- Polynomial a106 0.05 8.3 b106 0.16 58.5 Table 3. Linear regression parameters for in vitro development of eggs and pu- c 0.0012 0.0125 pae of Xyleborus glabratus over a range of constant temperatures 1628 C. d 0.016 0.091 e .3 5.3 Life stage r2 0.88 0.92 RSS 0.403 0.3136 Parameter Egg Pupa AIC 88.0 1.54 Intercept SE 0.264 0.02 0.163 0.02 Ratosy b 0.0264 0.018 Slope SE 0.011 0.01 0.0146 0.01 T0 14.4 6.3 aP value < 0.0001 < 0.0001 Tm 3.6 32.2 b Tmin 13.8 C 11.1 C c 0.14 3. c K 52.1 DD 68.2 DD r2 0.88 0.46 d 2 r 0.65 0.62 RSS 0.51 0.436 e RSS 0.5165 0.3139 AIC .3 866.2 fAIC 84.0 31.0

r rate of development; T treatment temperature ; T0 loer temperature threshold; a P value from the test of signicance of the regression coecient Tm lethal maimum temperature; Topt optmum temperature; r development rate at b Tmin intercept slope; T represents the loer temperature threshold epressed in C optmal temperature; D no. of degrees above the base temperature over hich thermal cK 1 slope; K represents the thermal constant epressed in degree-days DD inhibiton becomes predominant; m empirical constant; l empirical constant hich forc- dr2 represents the coecient of determinaton es the curve to intercept the y-ais at a value belo ero; a, b, c, d, e empirical constant; e 2 RSS represents the residual sum of suares Rm maimum development rate; r coecient of determinaton; RSS residual sum of fAIC represents the Aaie informaton criterion value suares; AIC Aaie informaton criterion value. 860 2015 — Florida Entomologist — Volume 98, No. 3 velopment as observed at 12 and 36 C. Mean development tmes culionidae developed at 12.5 to 35.0 C, and pupae developed at 12.5 for pupae ranged from 6.4 0.26 d at 32 C to 12. 0.51 d at 16 C to 3.0 C, hen eposed to constant temperatures ranging from 10 C Table 2. Development tmes for the pupal stages decreased from 16 to 3.5 C agner et al. 18, 188. Identcal trends of development to 28 C and then increased at 32 C. In the temperature range from ere observed ith avulsus Eichho Coleoptera: Curculionidae 16 to 28 C, linear regression yielded a loer temperature threshold of egg and pupal stages, ith development occurring from 15 to 35 C 11.1 C, ith the pupal stage reuiring 68.2 DD to develop to the adult hen observed at constant temperatures ranging beteen 10 and 35 stage Table 3. C agner et al. 188. Thus, X. glabratus egg and pupal development All nonlinear models gave a good t ith r2 values above 0.8 ith range temperatures ere similar to those of other scolytne species. the ecepton of the modied Lactn model, hich gave a poor t ith ne of the obectves as to select the mathematcal model that an r2 value of 0.34. All the evaluaton parameters, ed coecients, ould best eplain the temperature-dependent development of X. gla- and evaluaton criteria indices are presented in Table 4. The optmal bratus. e tested 1 linear and nonlinear models on ho ell they temperature of development of the pupal to adult stage ranged from describe the relatonships beteen temperature and the development 2.4 C Taylor model to 33.4 C Briere-1 model. The Briere-1, Logan, rates of eggs and pupae. Linear correlaton of the development rates of and polynomial models gave beer ts based on a greater r2 value and X. glabratus eggs and pupae ith temperatures beteen 16 and 28 C smaller RSS and AIC values. The Taylor model as a good t based resulted in estmated loer developmental threshold temperatures of on a greater r2 value and loer RSS and AIC values, but its estmated 13.8 C and 11.1 C for eggs and pupae, respectvely. In contrast, the loer development thresholds ere less than the observed values. estmated loer developmental threshold temperatures for egg and

The Logan model provided the best estmates of Tma 33. C and Topt pupal stages ere 15. C and 14.3 C, respectvely, for X. fornicatus 28. C. algama aluci 200a and 10.6 C and . C, respectvely, for Ips typographus L. Coleoptera: Curculionidae ermelinger Seifert LIFE CCLE AND DEELPMENT F X. GLABRATUS IN ACA 18. The loer threshold temperatures estmated by the linear mod- el for the temperature-dependent development of eggs ere close to D LGS AT CNSTANT TEMPERATURES the observed values, but the estmates for the pupal stage ere belo Xyleborus glabratus successfully completed its life cycle in avocado the loest temperature tested eperimentally. This discrepancy might logs held at temperatures of 24, 28, and 32 C. There as no develop- be due to nonlinear relatonships beteen temperature and develop- ment observed at 16 C. Temperature had a signicant eect on the ment rate near the threshold temperatures agner et al. 11. development of egg stage F 10.8; df 3, 14; P 0.0006, larval stage In the present investgaton, e evaluated the performance of

F .66; df 3, 16; P 0.0021, pupal stage F 12.6; df 3, 13; P = nonlinear models to describe the development of egg and pupal stages 0.0004, and teneral adults F 6.33; df 2, 14; P 0.01 in avocado of X. glabratus. The Briere-2, Ratosy, polynomial, and Logan mod- logs placed at dierent constant temperatures ranging from 16 to 32 C els gave good ts for the temperature-dependent development of eggs Table 5. The mean number of days to rst occurrence of each devel- as indicated by greater r2 and smaller RSS and AIC values, but the Logan opmental stage in avocado logs held at various constant temperatures model gave estmates that ere closest to the actual observatons. For is presented in Table 5 and Figs. 1 to 4. The largest numbers of eggs, temperature-dependent development of the pupal stage, the Briere-1, larvae, and teneral adults ere encountered at 28 C, folloed by 24, Logan, and polynomial models each gave a good t, ith the Logan 32, and 20 C Table 6. The largest numbers of pupae ere observed model giving estmates closest to the observed values. The Logan mod- at 24 C folloed by 28, 32, and 20 C. el proved to be the best model based on the evaluaton criteria and its closeness of estmated values of parameters to the actual observed values. In contrast, the Lactn model gave the best t for temperature- Discussion dependent development of X. fornicatus as compared ith other mathematcal models tested algama aluci 200b, hereas the The results from the current investgaton suggest that duraton of Lactn model proved least t to describe the temperature-dependent life cycle and development tme of immature stages is strongly related development of the egg and pupal stages of X. glabratus. The Briere-1 to temperature. e eposed egg and pupal stages of X. glabratus to model gave the best t for the temperature-dependent development constant temperatures ranging from 12 to 36 C. Egg and pupal develop- of E. lignosellus as indicated by a larger r2 value and smaller RSS and ment ere similar, as reported for Xyleborus fornicatus Eichho Gadd AIC values Sandhu et al. 2010. Eamples of best t for development 14; algama aluci 200a. For instance, X. fornicatus eggs and rates include the folloing: Logan model for Helicoverpa zea Boddie pupae did not develop at 15 C; hoever, X. fornicatus eggs and pupae Lepidoptera: Noctuidae Coop et al. 13, Briere-2 model for P. xy- developed hen held at 18 to 32 C Gadd 14; algama aluci lostella Goliadeh et al. 200, Lactn 2 model for Sesamia nonagri- 200b. Lieise, eggs of Germar Coleoptera: Cur- oides Lefbvre Lepidoptera: Noctuidae Fantnou et al. 2003, and

Table 5. Mean SE number of days to rst occurrence of each developmental stage of Xyleborus glabratus in avocado Persea americana logs held at constant temperatures. Results are based on the rst observaton of each developmental stage in avocado logs dissected at 2 d intervals.

Means SE of developmental period in days aer gallery initaton

Temperature C Eggs Larvae Pupae Adults 20 23 1.0 a 25.6 0. a 3.0 1.4 a 24 14.8 0.6 bc 20.3 1.4 b 26.4 2.1 c 31.6 1. ab 28 12.3 0.8 c 16.3 0. c 24.8 2.6 c 2. 0. b 32 16.4 0.5 b 18.8 0.8 bc 32.0 5.0 b 35.3 1.3 a

Means folloed by the same leer are not signicantly dierent based on the Tueyramer test for dierence of means P 0.05. No development as observed at temperatures here there are no values given. Brar et al.: Temperature-dependent development of the redbay ambrosia beetle 861

Fig. 1. Mean SE number of eggs per 5 galleries per log observed Fig. 2. Mean SE number of larvae per 5 galleries per log observed every other day in the avocado logs at 4 constant temperatures. every other day in the avocado logs at 4 constant temperatures. 862 2015 — Florida Entomologist — Volume 98, No. 3

Fig. 4. Mean SE number of teneral adults per 5 galleries per log encountered every other day in the avocado logs at 4 constant tem- peratures.

Briere-1 and Briere-2 models for C. pomonella Aghdam et al. 200. The variability in the performance of dierent mathematcal models to describe the temperature-dependent development of insects might be due to variability in thermal adaptatons of dierent insect species Sandhu et al. 2010, but the uality of the data set, especially data near the upper and loer developmental thresholds, also infuences model ng. Future studies are arranted to study temperature-dependent de- velopment of larval stages of X. glabratus along ith its symbionts at dierent constant temperatures. Moreover, avocado is not considered the preferred host for X. glabratus, and it is important to determine the Fig. 3. Mean SE number of pupae per 5 galleries per log encoun- development of X. glabratus on other host plants such as P. borbonia tered every other day in the avocado logs at 4 constant temperatures. and P. pallustris that support denser beetle infestatons than avocado. Brar et al.: Temperature-dependent development of the redbay ambrosia beetle 863 Table 6. Total number of Xyleborus glabratus of each developmental stage observed in dissected avocado Persea americana logs held at constant temperatures. Results are based on observatons in logs dissected at 2 d intervals for 40 d aer gallery initaton.

No. observed at each developmental stage

Temperature C Eggs Larvae Pupae Teneral adults 20 1 20 3 0 24 80 106 62 11 28 121 251 55 33 32 50 84 15 1

e hypothesie that redbay ambrosia beetle ill have more genera- Gadd CH. 14. bservatons on the life cycle of Xyleborus fornicatus Eichho in tons per year at loer lattudes compared ith higher lattudes. The the artcial culture. Annals of Applied Biology 34: 1-206. Goliadeh A, amali , Fathipour , Abbasipour H. 200. Temperature-depen- arm conditons in the southeastern United States and availability of dent development of diamondbac moth, Plutella xylostella Lepidoptera: dierent host trees may be infuencing the more rapid range epansion Plutellidae on to brassicaceous host plants. Insect Science 14: 30-316. of the redbay ambrosia beetle than predicted by earlier models of och Gramling M. 2010. Potental eects of laurel ilt of the fora of North America. Smith 2008. Southeastern Naturalist : 82-836. Haac RA. 2003. Intercepted Scolytdae Coleoptera at U.S. ports of entry. Inte- grated Pest Management Revie 6: 185-2000. Acknowledgments Hanula L, Mayeld AE, Fraedrich S, Rabaglia R. 2008. Biology and host as- sociatons of the redbay ambrosia beetle, Xyleborus glabratus Coleoptera: Curculionidae: Scolytnae, eotc vector of laurel ilt illing redbay Persea e gratefully acnoledge Stephen McLean Entomology and borbonia trees in the southeastern United States. ournal of Economic En- Nematology Department, University of Florida for help in maintaining tomology 101: 126-1286. the redbay ambrosia beetle colony. e also gratefully acnoledge Hanula L, Ulysen MD, Horn S. 2011. Eect of trap type, trap positon, tme of the Hammoc Dunes Club Golf Course, Palm Bay Brevard County for year, and beetle density on captures of the redbay ambrosia beetle Co- leoptera: Curculionidae: Scolytnae. ournal of Economic Entomology104: alloing us to cut infested redbay and sampbay ood. e gratefully 501-508. acnoledge the assistance of ames Colee IFAS Statstcs, University Hoell F, Neven LG. 2000. Physiological development tme and ero develop- of Florida. 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