Abridged Life Tables for Cephalonomia stephanoderis and Prorops nasuta (Hymenoptera: Bethylidae) Parasitoids of Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) Reared on Artificial Diet

Abridged Life Tables for Cephalonomia stephanoderis and Prorops nasuta (Hymenoptera: Bethylidae)... Biological aspects and demographic parameters of Cephalonomia stephanoderis Betrem (Hymenoptera: Bethylidae) and Prorops nasuta Waterston (Hymenoptera: Bethylidae) parasitoids of the coffee berry borer (CBB), Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) were investigated using diet-reared CBB hosts. Developmental time from eggs to adults, oviposition, and postoviposition period were comparable for both parasitoids. However, P. nasuta had a considerably longer preoviposition and longevity period averaging 17.3 and 63.1 d, respectively. The reproductive rate for C.  stephanoderis was 46.1 daughters per female with a mean generation time of 47.4 d, whereas P. nasuta had a reproductive rate of 18.3 daughters per female in a mean time of 58.6 d. Oviposition behavior was also different with C. stephanoderis typically ovipositing on CBB prepupae and pupae, while P.  nasuta preferred prepupae and second-instar CBB larvae. An abridged cohort life table for both parasitoids was constructed for growth rates estimations. Key words: Cenibroca diet, Cephalonomia stephanoderis, Prorops nasuta, African parasitoids, life table The coffee berry borer (CBB), Hypothenemus hampei (Ferrari) coffee berries or parchment coffee rearing methods). However, field (Coleoptera: Curculionidae: Scolytinae), is a key pest in coffee studies have demonstrated establishment under field condition (Coffea arabica L.) worldwide. Management of CBB has tradi- years after release for both C.  stephanoderis and P.  nasuta (Puzzi tionally been accomplished through IPM including sampling and 1939, Benassi 1995, Portilla and Bustillo 1995, Bustillo et al. 1996, monitoring, cultural harvesting, postharvest control, pest manage- Aristizabal et al. 1998, Quintero et al. 1998), showing promises as a ment during ‘zoqueo’, use of Beauveria bassiana, and release of management tool for CBB control. parasitoids (Aristizabal et  al. 2016). A  great interest exists in the Information on the parasitoids’ life histories has been studied potential for mass rearing of African parasitic wasps to reduce the by Abraham et al. (1990); Infante et al. (1992, 1994); Infante and damage produced by this pest. Among the most recognized bio- Barrera (1993); Bustillo et al. (1996); Portilla (1999a); Portilla and logical control agents are the parasitoids, Cephalonomia steph- Streett (2008); Portilla et al. (2014); and Vijayalakshmi et al. 2014. anoderis Betrem (Hymenoptera: Bethylidae) and Prorops nasuta The females enter the coffee berry and feed on CBB eggs, larvae, Waterston (Hymenoptera: Bethylidae). The practical use of P. nasuta prepupae, and adults. It appears that females for both C.  stephan- and C. stephanoderis in biological control programs began in 1929 oderis and P.  nasuta must feed on larvae or prepupae in order to and 1988, respectively. Murphy and Moore (1990), Portilla and develop eggs (Portilla and Streett 2008). The preoviposition period Bustillo (1995), Bustillo et  al. (1996), Portilla and Streett (2008), for both species lasts for several days (Murphy and Moore 1990). and Aristizabal et al. (2011) reported that in coffee producing coun- C.  stephanoderis eggs are normally oviposited on the ventral sur- tries where CBB is causing economic damage, these parasitoids have face of CBB larvae and prepupae and the dorso-abdominal region been reared under laboratory conditions and subsequently released. of the pupae. P.  nasuta exhibited no marked oviposition site pref- Nevertheless, to date, no classical introduction has provided satis- erence for deposition (Abraham et  al. 1990, Portilla et  al. 2014). factory control due to the large numbers of parasitoids required to Lateral-abdominal oviposition only on prepupa has been reported be released per infested coffee berries. Such demand for parasitoids for P. nasuta (Waterson 1923; Hargreaves 1926, 1935; Puzzi 1939; is quite high to be supplied with in vivo rearing (naturally infested Toledo 1942; Abraham et  al. 1990; Murphy and Rangi 1991), Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/ open-government-licence/version/2/). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Journal of Insect Science, 2018, Vol. 18, No. 2 whereas pupae and prepupae have been reported for C. stephanod- Materials and Methods eris (Infante 1993, Portilla 1999a). Insect Colonies Mass production of these parasitoids is directly linked to This study was conducted at the USDA-ARS, Biological Control of CBB host production, and life tables for both parasitoid and pest Pests Research Unit (BCPRU), Starkville, MS. Adults of CBB and are important to gain a better understanding on how to maintain parasitoids were from colonies established in 1999 (Portilla et  al. equilibrium without a negative impact in one or both populations 2014) and maintained previously in the National Research Center (Portilla et al. 2014). For example, complete and abridged life tables of Coffee (CENICAFE) in Chinchina, Colombia. The colonies were can be used for parasitoids depending on their oviposition behavior shipped to the quarantine facility, Stoneville, MS, in 1999. The para- as endoparasitoids, ectoparasitoids, or if they attack single or mul- sitoids and their host were reared according to the methods described tiple stages (Carey et al. 1988). There are a number of exceptions, by Portilla and Streett (2008). Rearing occurred in an environmental including C. stephanoderis, and P. nasuta, that attack larvae, prepu- room with a photoperiod of 16:8 (L:D) h, 27°C (±1.5°C), and 55 pae, pupae, and sometimes pharate adults (Portilla 1999a). C. steph- (±10%) RH (Portilla 1999a). The Cenibroca diet was used to rear anoderis and P.  nasuta are idiobionts ectoparasitoids, which allow CBB and was prepared according to the procedures found in Portilla construction of complete cohort life tables. However, on the rate of and Streett (2006). increase and demographic parameters such as net maternity, there is little available information. Infante et al. (1993) and Portilla (1999a) Biological Parameters of C. stephanoderis and found that fecundity and survivorships were largely affected by the P. nasuta extremes of temperature; high mortality was found in immature Cohorts of 291 recently parasitized hosts by C.  stephanoderis and stages for C.  stephanoderis at 17°C, while at 37°C, all specimens 547 recently parasitized hosts by P. nasuta were used for this study. died. The longevity was inversely related to temperature, although The size of cohort depended on availability. Each cohort was divided fecundity rate was reduced (Portilla 1999b). into 13 subcohorts (replicates) and placed into rearing containers Studies conducted in Colombia demonstrated that CBB could be (20 and 40 parasitized hosts per container, respectively) (Pioneer controlled in commercial coffee farms using inoculative and inun- plastic 032C, Dixon, KY). They were held inside the environmental dative releases of the African parasistoid C.  stephanoderis, when chambers (16:8 [L:D] h photoperiod, temperature of 25°C, and 55% the infestation is lower than 5% (20 wasps every 2 mo per infested RH) and kept until the last adult was obtained. Parasitized hosts berry) (Salazar et al. 2002). Portilla (1999c) based on the results of were observed every day. Total number of parasitoids surviving from Salazar et al. (2002) assessed approximately how many wasps should egg through adult and adult emergence was recorded on a daily basis be used per releases by using a simulation model for improving eco- for each species. logical and economic recommendations for the control of the CBB in Twenty-five extra hosts recently parasitized by C.  stephanoderis Colombia (Developed by Adrian Leach funded by The Department and P. nasuta were individually placed into Petri dishes 25 × 11 mm for International Development, United Kingdom) (Portilla 1999c). (Thermo Fisher 121V) and observed daily to determine egg, larva, She gave the following example: The coffee harvest distribution of a prepupa, and pupa developmental time. From the 13 groups of each hectare of 5,000 coffee trees with approximately 1,500 ripe berries species, 15 copulated females were taken and individually confined per tree and 5% of CBB infestation would need about 4,400,000/ into larger Petri dishes (35 × 11 mm) that contained 30 CBB immature ha (20 wasps per infested berry) to keep the CBB population under stages (10 second-instar larvae, 10 prepupae, and10 pupae) for ovipo- the threshold (2% of infestation). These wasps would be distrib- sition as well as few eggs and first-instar larvae for feeding. The num- uted through the year with releases every 2 mo as follow: February ber of eggs oviposited every day by each parasitoid of both bethylids (260,000 wasps/ha), April (100,000 wasps/ha), June (480,000 wasps/ were counted and recorded until the last wasp was dead. Petri dishes ha), August (380,000 wasps/ha), October (2,000,000 wasps/ha), and were cleaned daily removing any dead or parasitized hosts and replac- December (1,200,000 wasps/ha). Producing those large numbers ing them with new ones. Means of number of eggs oviposited per each of parasitoids in a cost-effective way will depend on well-designed female, longevity, pre-post, reproductive, and reproductive periods of production facilities using industrial level mechanized and auto- C. stephanoderis and P. nasuta and their host preference for ovipos- mated rearing processes only. Portilla 1999a and Portilla and Streett iting were determined. The progeny of each female was maintained 2008 reviewed and discussed the requirements for a semiautoma- until adult emergence when sex ratio was determined. tion system for mass production of CBB and its African parasitoids including diet preparation, sanitation, environmental factors, qual- Demographic Parameter of C. stephanoderis and ity control, storage, and distribution. Unfortunately, no studies have P. nasuta examined calculation costs between the in vivo (naturally infested berries or parchment coffee methods) and the in vitro (artificial diet) Abridged life tables for both species of parasitoid were calculated rearing system for parasitoids production. However, to the best of according to Portilla et al. (2014). Immature survival was calculated our knowledge, no in vivo rearing system currently available will be using the subcohorts for each parasitoid species. The fraction of able to supply such demand. death was calculated by the sum of all dead in each developmental This study was conducted to obtain information on the bio- stage and divided for the total beginning stages (synthetic cohort). logical parameters and fertility rates of these parasitoid species in This value was used for incorporating in the adult survival parame- an effort to get a better understanding how to improve our ability to ter (l ). Data obtained for the number of parasitic females alive each rear large numbers for field release. Parasitoids were reared on CBB day at each age (x) and the number of eggs oviposited each day were using Cenibroca artificial diet. Abridged cohort life tables for both used to calculate the basic population parameters: gross maternity parasitoids were constructed for growth rate estimations. Results (M ), survival (L ), fecundity (m ), net maternity function (l .m ), x x x x x are presented with tables and figures with a detailed description net reproductive rate (R ), finite rate of increase (λ), intrinsic rate of all biological factors obtained by daily observations in life-table of increase (r ), mean generation time (T), and doubling time (DT) construction. (Krebs 2001, Pressat 1985, Carey 1993). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 3 parasitoids had a marked difference in survival between species for Statistical Analysis both eggs (F = 11.17; df = 1, 24; P = 0.0027) and pupae (F = 23.70; One-way analysis of variance and the Tukey’s Honest Significant df = 1, 24; P = 0.0001), while no differences in survival were observed Difference test (SAS Institute, 2013) were used to compare life-ta- for larvae (F = 4.21; df = 1, 24; P = 0.0512) (Table 2) . A comparison ble parameters, developmental time, preoviposition and oviposi- of female progeny production among species revealed that C. steph- tion period, longevity, immature mortality, and host preference. anoderis had a significantly higher reproduction than that of P.nasuta Nonparametric estimates of the survival function of females were (F = 15.95; df = 1, 28; P = 0.0004). There were significant differences compered between parasitoid species by using PROC LIFETEST test in female production per day (F = 151.85; df = 1, 940; P = 0.0001), procedure in SAS (SAS 2013). Regression analysis was used to deter- where C. stephanoderis female were found ovipositing 2.22 ± 0.06 mine differences in cumulative gross fecundity between C. stephan- (SE) eggs/day/female and P. nasuta 1.21 ± 0.06 (SE) eggs/day/female. oderis and P. nasuta. In general, both parasitods species were normally found ovipositing from one to three eggs per day. However, sporadic ovipositions from Results four to seven eggs per day were observed for C. stephanoderis and from four to five eggs per day for P.  nasuta. The number of eggs Biological Parameters of C. stephanoderis and per wasp varied from 38 to 114 eggs for C.  stephanoderis and 6 P. nasuta to 88 eggs for P.  nasuta. Suggesting that it could be related to the The percentages of host parasitized being offered equal numbers of amount of CBB stages provided during their entire life (about 300 second instar larvae, prepupae, and pupae of CBB of both parasi- CBB stages). Percentage of number of eggs oviposited per female toids are presented in Fig. 1. C. stephanoderis had high percentages among species is presented in Fig. 2. No C. stephanoderis population of parasitism in prepupae (60.85 ± 11.67 [SE]) followed by pupae was found with <20 eggs per wasp and 0% of P. nasuta population (36.61 ± 11.28 [SE]) and only small populations of parasitized sec- had >100 eggs per parasitoid. In total, 20% of C. stephanoderis and ond-stage larvae were observed (2.52 ± 1.77 [SE]), whereas P. nasuta 55% of P. nasuta population was found ovipositing 20–50 eggs per had a high preference for prepupae (50.29  ±  13.47 [SE]) followed female, while 53% of C. stephanoderis and 20 % of P. nasuta popu- by second-instar larvae (45.07 ± 14.72 [SE]) and occasionally par- lation was found ovipositing 50–100 eggs per female. asitized pupae were observed (4.63 ± 3.15 [SE]). There were signifi- Both parasitic wasps had a different behavior on host parasitisa- cant differences among preferences of parasitism percentage (df = 1, tion. C. stephanoderis oviposited a single egg per host and did not 28; P = < 0.0001; F = 123.33, 5.49, 79.15 for second-instar larvae, oviposit until the host was completely paralysed, whereas P. nasuta prepupae, and pupae, respectively). The developmental time to egg could oviposited more than one egg on host when they still moving, (F = 80.93; df = 1, 48; P = 0.0001), larvae (F = 11.19; df = 1, 48; although the host have had various stinging. This behavior could P  =  0.0016), and cocoon (F  =  32.05; df  =  1, 48; P  =  0.0001) was explain the statistic differences found on their pre-reproductive significantly different among species. There were no statistical dif- period (F = 16.56; df = 1, 28; P = 0.0003) and longevity (F = 7.55; ferences for prepupae (F = 0.05; df = 1, 48; P = 0.8295) and pupae (F  =  0.91; df  =  1, 48; P  =  0.3437) between parasitoids (Table  1). Cocoons were formed in 2 d for both parasitoid species. No Table  1. Mean developmental time for the immature stages of C. stephanoderis and P. nasuta developed on diet-reared CBB hosts cocoons were formed in 51.65% of C.  stephanoderis’s population and 42.46% of P.  nasuta, but individuals still developed to adult Life stages Developmental times (d) (Mean ± SE) maturity. The proportion of death in each immature stage of C. stephan- C. stephanoderis P. nasuta oderis and P. nasuta is presented in the Table 2. Using GLM analysis, Egg 3.00 ± 0.58a 4.48 ± 0.49b Larva 4.16 ± 0.84a 4.96 ± 0.63b Cocoon 3.84 ± 0.62a 2.84 ± 0.51b Prepupae 4.08 ± 0.65a 4.12 ± 0.53a Pupa 13.60 ± 1.03a 13.32 ± 0.85a Total time to adult 28.68 ± 1.58a 29.72 ± 1.05b Means ± SE followed by the same letter in each row are not significantly different (P < 0.05, Tukey’s test) (N = 25 per species). Table  2. Immature stage mortality for C.  stephanoderis and P. nasuta developed on diet-reared CBB hosts Stages/parameters Percentage immature mortality (mean ± SE) C. stephanoderis P. nasuta Eggs 4.17 ± 4.08a 12.33 ± 7.10b Larvae 11.09 ± 6.31a 17.93 ± 9.74a Pupae 1.4 ± 1.89a 12.61 ± 7.53b Cumulative mortality 16.12 ± 6.98a 36.31 ± 14.66b Survival to adulhood 83.87 ± 6.42a 63.69 ± 15.08b Fig.  1. Hosts preference percentage parasitized by C.  stephanoderis and P.  nasuta. Bars not sharing the same uppercase letter are significantly Means + SE followed by the same letter in each row are not significantly different. (Tukey’s test P = 0.05) (means ± SE). different (P < 0.05, Tukey’s test). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2018, Vol. 18, No. 2 df = 1, 28; P = 0.0104). Preoviposition period (17.26 ± 10.57 d) and X  = 11.10, df = 1, P < 0.0009) (Fig. 3B). Differences in the cumu- longevity (63.13 ± 13.23 d) were significantly longer for P.  nasuta lative gross fecundity, indicating a logarithmic regression type with as compared to C.  stephanoderis, (4.25 ± 0.43 and 46.66 ± 15.41 r values of 0.997 and 0.979 for C.  stephanoderis and P.  nasuta, d). GLM showed no significant differences among parasitoids on respectively, is illustrated in Fig. 3C. reproductive (F = 0.83; df = 1, 28; P = 0.3706) and postreproductive Seven life-table parameters are presented in Table 5. The higher periods (F = 3.98; df = 1, 28; P = 0.0559) (Table 3). During their pos- gross fecundity occurred for C.  stephanoderis with 73.06  ±  26.22 treproductive period both wasp species continued feeding upon their (SE) eggs per wasp, while 35.93  ±  24.68 (SE) eggs per wasp was hosts. Both parasitoid species tended to produce more females than obtained to P. nasuta. Finite rate of increase (λ) is the factor by which males, but their sex ratio varied among species. Total eggs deposited a population increases each day and is determined by the intrinsic by C. stephanoderis and P. nasuta and sex ratio among paratitoids rate of increase (r ). C. stephanoderis had the highest finite rate of are presented in Table 4. increase. The growth rate per generation of C.  stephanoderis was 46.15 female wasps per newborn female with a mean time of 47.39 d. The daily growth rate was 1.09 daughter females per female, dou- Life-Table Parameter of C. stephanoderis and bling this number in 6.5 d. The growth generation for P. nasuta was P. nasuta 18.33 daughter females per female with a mean time of 58.60 d; its Life-table data indicated differences between the two parasitoid spe- daily growth rate was 1.05 females per female doubling this number cies. For example, mean daily egg production (M ) for C. stephanod- in 13.12 d. eris increased to almost 4.0-fold during the first week and remained at high numbers of egg production until the end of the second week (Fig.  3A). Subsequently, the production of this parasitoid declined Discussion over the next 5- to 6-wk period reaching zero by about day 50. The parasitic wasps C.  stephanoderis and P.  nasuta are idiobionts Alternatively, P. nasuta showed a constant trend in production from ectoparasitoids that attack every stage of CBB ovipositing on final- day 19 to day 45. Mortality, analyzed by the test of equality with stage larvae (2.52 and 45.07%), prepupal (60.85 and 50.29%), and the strata statement in –log (survival probability) PROC LIFETEST, the pupal stages (36.61 and 4.63%), respectively, which is quite indicated significant differences among parasitoids (Log-Rank common among idiobiont ectoparasitoids (Shaw 1994). Both par- asitoids preferred to feed on pupae rather than eggs or early instar larvae. The percentages of host preference obtained in this work differ from Barrera et  al. (1989) and Abraham et  al. (1990) who found that C.  stephanoderis preferred ovipositing on pupae rather than prepupae. However, Infante (1993) observed 55.4% of eggs on prepupae and 44.6% on pupae. Portilla (1999) found similar results for C. stephanoderis, which was exposed to different temperatures . Lateral-abdominal oviposition occurring only on prepupa has been reported for P. nasuta by Waterson (1923); Hargreaves (1926, 1935); Puzzi (1939); Toledo (1942); Abraham et  al. (1990); and Murphy and Rangi (1991). Oviposition was never seen on prepupa except by Toledo (1942). In this study, P. nasuta was found ovipositing eggs on the dorso-abdominal of the pupa and in a variety of areas on both prepupa and second-instar larval of CBB. There are two general forms of the life table, using original or hypothetical cohorts (Carey 1993). The first is the cohort life table, which provides a longitudinal perspective that includes the mortality experience of a particular cohort from the moment of birth through consecutive ages until no individuals remain in the original cohort. The second is the abridged life table, which assumes a hypothetical Fig. 2. Population percentage of C. stephanoderis and P. nasuta oviposition cohort subject throughout its lifetime to the age-specific mortality number of eggs per female (n = 15 parasitoid females). rates prevailing for the actual population over a specific period. Most aspects of the life history of C.  stephanoderis and P.  nasuta Table  3. Preoviposition, oviposition, and postoviposition periods, have been collected from studies carried out in captivity using a and longevity of C. stephanoderis and P. nasuta developed on diet- reared CBB hosts Table  4. Total production and sex ratio of C.  stephanoderis and Periods Developmental (Means + SE) P. nasuta developed on diet-reared CBB hosts times (d) Variable Parasitoids C. stephanoderis P. nasuta C. stephanoderis P. nasuta Preoviposition 4.53 ± 0.43a 17.26 ± 10.57b Oviposition 32.13 ± 13.16a 28.40 ± 8.42a Total eggs oviposited 1,101 540 Postoviposition 11.00 ± 8.54a 17.46 ± 8.58a Total adult emerged 815 388 Adult longevity 47.66 ± 15.41a 63.13 ± 13.23b Total females 702 302 Total males 113 86 Means ± SE followed by the same letter in each row are not significantly Sex ratio 6.2:1 3.5:1 different (P = 0.05, Tukey’s test) (N = 15 per species). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 5 Table  5. Life-table statistic for C.  stephanoderis and P.  nasuta reared on H. hampei developed on diet-reared CBB hosts Parameters and units Parasotoids C. stephanoderis P. nasuta Gross fecundity (M ) 81.32 39.44 Fecundity (m ) 67.99 31.09 Net reproductive rate (R ) 46.15 18.33 Mean generation time (T) 47.39 58.60 Doubling time (DT) 7.78 13.12 Intrinsic rate of increase 0.089 0.052 Finite rate of increase (λ) 1.09 1.05 Total offspring/female. Females/female at age x. Daughters/new-born female (Population which increases each generation). Mean age of reproduction (d). Time required for (λ) to doubling number. Rate of natural increase (daughters/female/day). Individuals/female/day. for preoviposition and 30.6 d from egg to adult at 27ºC and 75% RH. At 25ºC and 90% RH, Abraham, et al. (1990) obtained a pre- oviposition period of 14 d and development time of 22.4 d at 25°C. The statistical analysis of the synthetic cohort used for C. steph- anoderis and P. nasuta permitted the construction of abridged life-ta- ble functions, which were computed daily over their entire life. The development time from egg to adult did not vary appreciably from results obtained by different researchers with temperatures of 25°C. P.  nasuta had a higher mortality value for every immature stage in comparison to C.  stephanoderis (Table  2). The low mortality of C. stephanoderis is probably reflected in the ability of the female to select high-quality hosts (large and healthy) for oviposition, whereas P. nasuta was observed ovipositing eggs on larvae when the paraly- sis process was uncompleted. The capacity of predation of P. nasuta is another characteristic that impacts mortality, due to the female ovipositing eggs on the host where predation was initiated and even oviposited on small larvae. In effect, this type of stage selection does not provide all the resources necessary for its survival. These behav- ioral characteristics for P. nasuta provide a better understanding why this parasitoid has been difficult to rear under laboratory conditions. Portilla (1999a) reported only 28.4 stages per parchment coffee at 25 d after infestation, and from this population only a 29.09% has the probability to be parasitized by C. stephanoderis. This percentage Fig.  3. Life-table data of C.  stephanoderis and P.  nasuta restricted to adult would be lower if the same population was parasitized by P. nasuta. stage. (A) gross fecundity (Mx); (B) survival (lx); and (C) regression of In captivity, and under good conditions, many wasp species will cumulative gross fecundity. live 1 or 2 mo (Quicke 1997) . Barrera et al. (1989) investigated the effect of adult diet on longevity of C.  stephanoderis. He mentioned hypothetical cohort. This is because under normal circumstances, its that longer longevity was found (77 d) when the adults were procided complete life cycle is not feasible. Several studies have reported com- a honey–water mixture. However, Murphy and Rangi (1991) reported parative data for different feeding regimes, temperatures, and some only 2 d for P. nasuta when fed honey and there were no significant aspects of oviposition behavior and reproductive potential. Koch differences when fed CBB pupas and adults with no additional food. (1973) showed that C.  stephanoderis has a developmental time of The same authors reported 14 d when P. nasuta was fed CBB eggs and 23.2, 20.0, 15.2, and 14.6 d at 24, 27, 30, and 32°C, respectively. larvae. The larger longevity of C. stephanoderis and P. nasuta found Also, the preoviposition time varied from 8.0 d at 21°C to 2.0 d in this study could be related to the amount of suitable hosts pro- at 27°C. However, 10 d at 17°C and 2 d at 32°C was the preovi- vided during their entire life (almost 300 CBB stages per female wasp). position period identified by Infante (1993). Portilla (1999) found Fecundity ranges enormously in parasitic wasps and depends upon that the preoviposition period occurred in 4.5 d at 23°C, 3.7, 2.9 several factors, including species, size, and diet (Jervis and Copland and 2.1 d at 25, 27, and 29°C, respectively. She also reported devel- 1996). Abraham et  al. (1990) found that female C.  stephanoderis opmental times of 28.1, 25.1, 23.2, and 19.9 d at 23, 25, 27, and could lay 1–3 eggs and occasionally 4 per day and produce up to 70 29°C, respectively. Eggs hatch varied from 4.1 d at 23°C to 2.9 d at eggs during her life. Barrera et al. (1989) found up to 9 eggs per para- 29°C, Abraham et al. 1990 found that at 25ºC eggs hatched in 1.61 sitoid per day and the most fecund individual produced 139 eggs in 66 d. Murphy and Rangi (1991) reported that P.  nasuta needed 5.3 d Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Journal of Insect Science, 2018, Vol. 18, No. 2 d. In this study, the numbers of eggs per C. stephanoderis varied from Aristizabal, L. F. and A. E. Bustillo, S. P. Arthurs. 2016. Integrated pest man- agement of coffee berry borer: strategies from Latin American that could 34 to 114, and from 6 to 88 to P. nasuta. C. stephanoderis, on average, be useful for coffee farmers in Hawaii. Insects. 7:1–24. oviposited 81 eggs per wasp in 47.6 d and in comparison, P. nasuta Baker, P. 1999. La broca del café en Colombia: informe final del proyecto MIP oviposited 47 eggs in 63.1 d.  These results indicate that under field para el café DFID—Cenicafe. CABI Bioscience, Ascot, United Kingdom. conditions, females of C.  stephanoderis and P.  nasuta never obtain enough hosts to achieve full reproductive potential. Several studies Barrera, J. F., A.  Castillo, F.  Infante, J.  Gómez, and W.  De La Rosa. 1989. confirmed that females always predominate in these two bethilides. Biologie de C. Stephanoderis (Betrem) (Himenóptera: Bethylidae) en lab- The field sex ratio of the parasitic wasp C. stephanoderis recorded by oratorio. Cicle bioloque, capasite de oviposition, et emergente du fruit du Ticheler (1961) was 4.8 females per 1 male, and Koch (1973) found cafeier. Café Cacao, The Francia. 33: 101–108. 2.7 females per 1 male. Barrera et al. (1993) obtained a sex ratio of 7:1 Benassi, V. L. 1995. Levantamiento dos inimigos naturais da broca du café under laboratory condition, while Benassi (1998) found a P nasuta a Hypothenemus hampei (Coleoptera: Scolytidae) no norte du Espiritu Santo. An. Soc. Entomol. 24: 635–638. sex ratio of 5.2 females per male. This ratio varied through various Bustillo, A., J. Orozco, P. Benavides, and M. Portilla. 1996. Producción masiva generations, with 28.5 females per male after five generations. The sex y uso de parasitoides para el control de la broca del café en Colombia. Rev. ratio obtained in this work was 6.2: 1 and 3.5: 1 for C. stephanoderis Col. Entomol. 47: 215–230. and P. nasuta, respectively. Carey, J. R. 1993. Applied demography for biologist with special emphasis on According to these results C.  stephanoderis produced more insects. Oxford University Press, Oxford, United Kingdom, p. 206. females per female than P. nasuta (R ), but both parasitoids need at Carey, J. R., T. Y. Wong, and M. M. Ramadan. 1988. Demographic framework less 50 suitable host stages to assure progeny. The speed at which the for parasitoid mass rearing: case study of Biosteres tryony (Hymenoptera: colony increased (r ) is the most important parameter, and C. steph- Braconidae), a larval parasitoid of tephritid fruit flies. Theor. Popul. Biol. anoderis obtained a high intrinsic rate of increase. Mass production 34: 279–296. of both parasitoids depends on the host reproductive potential, and Hargreaves, H. 1926. Notes on the Coffee berry bore. Bull. Entomol. Res. 16: 347–354. hence, these results provide insight as to why the parasitoids have Hargreaves, H., 1935. Stephanoderis hampei Ferr. Coffee berry borer in been so unsuccessful in the field, because to proliferate they evidently Uganda. East Afri. Agric. 1:218–224. need a range of host stages. If a wasp attacks an immature berry, it Infante, F. and L. J. Barrera. 1993. Estadísticos demográficos de Cephalonomia will encountered only eggs and young larvae which they may con- stephanoderis Betrem (Himenóptera: Bethylidae) a temperaturas con- sume and kill the CBB female as well, but the female parasitoid will stantes. Folia. Entomol. Mex. 87: 61–72. not produce any offspring (Baker 1999, Ruiz-Cardenas and Baker Infante, F., L. J. Barrera, J. Gomez, and A. Castillo. 1992. Thermal constants 2010). In addition, if the wasp arrives too late, they will find mostly for pre-marginal development of the parasitoid Cephalonomia stephanod- adult CBB and have to wait until they start breeding, by which time eris Betrem (Hymenoptera: Bethylidae). Can. Ent. 124: 935–941. harvest may intervene. All this suggests that C.  stephanoderis and Infante, F., J. Valdes, V. Penagos, and J. Barrera. 1994. Description of the life P. nasuta will be incompatible with efficient commercial production. stages of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), a par- asitoid of Hypothenemus hampei (Coleoptera: Scolytidae). Vedalia. 1: However, we must consider studies that have demonstrated that a 13–18. high number of wasps per hectare (20 wasps per infested berry every Jervis, M. A. and M. J.  Copland. 1996. The life cycle. In: M. A. Jervis and 6 mo) can control CBB or keep it under controls in plots with less N. Kidd (ed.), Insect natural enemies. Chapman and Hall, London. than 5% of CBB infestation (Aristizabal et  al. 1997, Salazar and pp. 63–161. Baker 2002, Aristizabal et al. 2011). Krebs, C. J. 2001. Ecology: the experimental analysis of distribution and abun- dance, 5th ed. Wesley Longman, San Francisco, CA. p. 695. Kock, V. J. 1973. Abondance de Hypothenemus hampei Ferr. Scolyte des graines Acknowledgments de café en function de sa plante hote et de son parasite Cephalonomia The authors would like to thank Luis Carlos Jojoa former technician at USDA, stephanoderis Betrem en Cote de’ Ivore. Medd. Landbou. 73: 1–85. ARS, BCPRU, Starkville, for their valuable support in rearing the host and par- Murphy, S. and D. Moore. 1990. Biological control of the coffee berry borer, asitoid colonies. We are also grateful to Carlos Blanco (SIMRU-ARS-USDA) Hypothenemus hampei (Ferrari) (Coleoptera, Scolytidae): previous pro- and Arnubio Valencia (Nebraska University, Department of Entomology) for grams and possibilities for the future. Biol. Control. 11: 107–117. critically reviewing an early version of this manuscript. Murphy, S. T. and D. K. Rangi. 1991. The use of the African wasp, Prorops nasuta for the control of the Coffee Berry Borer, Hypothenemus hampei in Mexico and Ecuador: the Introduction program. Insect. Sci. Applic. 12: References Cited 27–34. Abraham, Y. J., D. Moore, and G. Godwin. 1990. Rearing and aspects of biol- Portilla, M. 1999a. Mass rearing technique for Cephalonomia stephanod- ogy of Cephalonomia stephanoderis and Prorops nasuta (Hymenoptera: eris (Hymenoptera: Bethylidae) on Hypothenemus hampei (Coleoptera Bethylidae) parasitoids of the coffee berry borer, Hypothenemus hampei Scolytidae) developed using Cenibroca artificial diet. Rev. Col. Entomol. (Coleoptera: Scolytidae). Bull. Entomol. Res. 80:121–128. 25: 57–66. Aristizabal, L. F., P. S.  Baker, J.  Orozco, and B.  Chavez. 1997. Parasitismo Portilla, M. 1999b. Desarrollo y evaluación de una dieta artificial para la de Cephalonomia stephanoderis (Betrem) sobre una poblacion the cría masiva de Hypothenemus hampei (Coleoptera: Scolytidae). Rev. Col. Hypothenemus hampei (Ferrari) con niveles bajos de infestacion en Entomol. 1: 24–38. campo. Rev. Colomb. Entomol. 23:157–164. Portilla, M. 1999c. Mass production of Cephalonomia stephanoderis on Aristizabal, L. F., P. S. Baker, J. Orozco, and B. Chavez. 1998. Effecto del para- Hypothenemus hampei reared using artificial diet. Thesis. Univerisity of sitoide Cephalonomia stephanoderis (Hymenoptera: Bethylidae) sobre las London, England. 253 pp. poblaciones de Hypothenemus hampei (Coleoptera: Scolytidae) durante y Portilla, M. and A. Bustillo. 1995. Nuevas investigaciones en la cría masiva de despues de la cosecha. Rev. Colomb. Entomol. 24:149–155. Hypothenemus hampei y de sus parasitoides Cephalonomia stephanoderis Aristizabal, L. F., M.  Jimenez, A. E.  Bustillo, and S. P.  Arthurs. 2011. y Prorops nasuta. Rev. Col. Entomol. 21: 25–33. Introduction of parasitoids of Hypothenemus hampei (Coleoptera: Portilla, M. and D.  Streett. 2006. Nuevas técnicas de producción masiva de Scolytidae) on small coffee plantations in Colombia through farmer par- Hypothenemus hampei sobre la dieta artificial Cenibroca modificada. Rev. ticipatory methods development. Fla. Entomol. 94: 690–693. Col. Entomol. 57: 37–50 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 7 Portilla, M. and D.  Streett. 2008. Avances investigativos en la produc- Salazar, H. M. and P. Baker. 2002. Impacto de liberaciones de Cephalonomia ción masiva automatizada de la broca del café Hypothenemus hampei stephanoderis sobre poblaciones de Hypothenemus hampei. Rev. Col. (Coleoptera: Scolytidae) y de sus parasitoides sobre dietas artificiales. Sis. Entomol. 53: 306–316. Agroeco. Mod. Biomatematics. 1:9–12 SAS Institute. 2013. SAS/STAT user’s manual, version 9, 4th ed. SAS Institute, Portilla, M., J.  Ramos-Morales, G.  Rojas, and C.  Blanco. 2014. Life tables Cary, NC. as tools of evaluation and quality control for arthropods mas produc- Shaw, M. 1994. Parasitoid host range. In: B.A. Hanwkins and W. Sheeham tion. In: J. Morales-Ramos (ed.) Mass production of beneficial organisms, (eds.). Parasitoid community ecology, Oxford University Press, Oxford, pp. 241–275. Academic Press, New York. 742 pp. United Kingdom, pp. 11–144. Pressat, R. 1985. The dictionary of demography. Bell and Bain, Ltd., Glosgow. Ticheler, J. H. 1961. Ėtude analytique de l’ epidemiologie du scolyte des Puzzi, D. 1939. Valor du parasitismo da Prorops nasuta Waterson no cambate graines de café Stephanoderis hampei Ferr., en Côte d’ Ivore. Medde. a brocada cafe. J. Agrono. 2: 259–264. Landb. 61: 1–49. Quintero, C., A. E.  Bustillo, P.  Benavides, and B.  Chavez. 1998. Evidencia Toledo, A. A. 1942. Notas sobre a biologia da vespa de Uganda, Prorops del establecimiento de Cephalonomia stephanoderis y Prorops nasuta nasuta Waterson, (Hymenopera: Bethylidae) no estado de S. Paulo–Brasil. (Hymenoptera: Bethylidae) en cafetales del departamento de Nariño, Arqu. Inst. Biol. 13: 233–260. Colombia. Rev. Colomb. Entomol. 24:141–147. Vijayalakshmi, C. K., C. Simi, K. Tintumol, and P. K. Vinodkumar. 2014. Life Ruiz-Cardenas, R. and P.  Baker. 2010. Life table of Hypothenemus hampei cycle of the coffee berry borer parasitoid, Cephanolomia stephanoderis (Ferrari) in relation to coffee berry phenology under Colombian field con- (Hymenoptera: Bethylidae) on parchment and cherry coffee. Int. J. of Sci. ditions. Sci. Agric. 67: 658–668. Tech. Research. 3: 151–152. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Insect Science Oxford University Press

Abridged Life Tables for Cephalonomia stephanoderis and Prorops nasuta (Hymenoptera: Bethylidae) Parasitoids of Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) Reared on Artificial Diet

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Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US.
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Abstract

Biological aspects and demographic parameters of Cephalonomia stephanoderis Betrem (Hymenoptera: Bethylidae) and Prorops nasuta Waterston (Hymenoptera: Bethylidae) parasitoids of the coffee berry borer (CBB), Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) were investigated using diet-reared CBB hosts. Developmental time from eggs to adults, oviposition, and postoviposition period were comparable for both parasitoids. However, P. nasuta had a considerably longer preoviposition and longevity period averaging 17.3 and 63.1 d, respectively. The reproductive rate for C.  stephanoderis was 46.1 daughters per female with a mean generation time of 47.4 d, whereas P. nasuta had a reproductive rate of 18.3 daughters per female in a mean time of 58.6 d. Oviposition behavior was also different with C. stephanoderis typically ovipositing on CBB prepupae and pupae, while P.  nasuta preferred prepupae and second-instar CBB larvae. An abridged cohort life table for both parasitoids was constructed for growth rates estimations. Key words: Cenibroca diet, Cephalonomia stephanoderis, Prorops nasuta, African parasitoids, life table The coffee berry borer (CBB), Hypothenemus hampei (Ferrari) coffee berries or parchment coffee rearing methods). However, field (Coleoptera: Curculionidae: Scolytinae), is a key pest in coffee studies have demonstrated establishment under field condition (Coffea arabica L.) worldwide. Management of CBB has tradi- years after release for both C.  stephanoderis and P.  nasuta (Puzzi tionally been accomplished through IPM including sampling and 1939, Benassi 1995, Portilla and Bustillo 1995, Bustillo et al. 1996, monitoring, cultural harvesting, postharvest control, pest manage- Aristizabal et al. 1998, Quintero et al. 1998), showing promises as a ment during ‘zoqueo’, use of Beauveria bassiana, and release of management tool for CBB control. parasitoids (Aristizabal et  al. 2016). A  great interest exists in the Information on the parasitoids’ life histories has been studied potential for mass rearing of African parasitic wasps to reduce the by Abraham et al. (1990); Infante et al. (1992, 1994); Infante and damage produced by this pest. Among the most recognized bio- Barrera (1993); Bustillo et al. (1996); Portilla (1999a); Portilla and logical control agents are the parasitoids, Cephalonomia steph- Streett (2008); Portilla et al. (2014); and Vijayalakshmi et al. 2014. anoderis Betrem (Hymenoptera: Bethylidae) and Prorops nasuta The females enter the coffee berry and feed on CBB eggs, larvae, Waterston (Hymenoptera: Bethylidae). The practical use of P. nasuta prepupae, and adults. It appears that females for both C.  stephan- and C. stephanoderis in biological control programs began in 1929 oderis and P.  nasuta must feed on larvae or prepupae in order to and 1988, respectively. Murphy and Moore (1990), Portilla and develop eggs (Portilla and Streett 2008). The preoviposition period Bustillo (1995), Bustillo et  al. (1996), Portilla and Streett (2008), for both species lasts for several days (Murphy and Moore 1990). and Aristizabal et al. (2011) reported that in coffee producing coun- C.  stephanoderis eggs are normally oviposited on the ventral sur- tries where CBB is causing economic damage, these parasitoids have face of CBB larvae and prepupae and the dorso-abdominal region been reared under laboratory conditions and subsequently released. of the pupae. P.  nasuta exhibited no marked oviposition site pref- Nevertheless, to date, no classical introduction has provided satis- erence for deposition (Abraham et  al. 1990, Portilla et  al. 2014). factory control due to the large numbers of parasitoids required to Lateral-abdominal oviposition only on prepupa has been reported be released per infested coffee berries. Such demand for parasitoids for P. nasuta (Waterson 1923; Hargreaves 1926, 1935; Puzzi 1939; is quite high to be supplied with in vivo rearing (naturally infested Toledo 1942; Abraham et  al. 1990; Murphy and Rangi 1991), Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/ open-government-licence/version/2/). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Journal of Insect Science, 2018, Vol. 18, No. 2 whereas pupae and prepupae have been reported for C. stephanod- Materials and Methods eris (Infante 1993, Portilla 1999a). Insect Colonies Mass production of these parasitoids is directly linked to This study was conducted at the USDA-ARS, Biological Control of CBB host production, and life tables for both parasitoid and pest Pests Research Unit (BCPRU), Starkville, MS. Adults of CBB and are important to gain a better understanding on how to maintain parasitoids were from colonies established in 1999 (Portilla et  al. equilibrium without a negative impact in one or both populations 2014) and maintained previously in the National Research Center (Portilla et al. 2014). For example, complete and abridged life tables of Coffee (CENICAFE) in Chinchina, Colombia. The colonies were can be used for parasitoids depending on their oviposition behavior shipped to the quarantine facility, Stoneville, MS, in 1999. The para- as endoparasitoids, ectoparasitoids, or if they attack single or mul- sitoids and their host were reared according to the methods described tiple stages (Carey et al. 1988). There are a number of exceptions, by Portilla and Streett (2008). Rearing occurred in an environmental including C. stephanoderis, and P. nasuta, that attack larvae, prepu- room with a photoperiod of 16:8 (L:D) h, 27°C (±1.5°C), and 55 pae, pupae, and sometimes pharate adults (Portilla 1999a). C. steph- (±10%) RH (Portilla 1999a). The Cenibroca diet was used to rear anoderis and P.  nasuta are idiobionts ectoparasitoids, which allow CBB and was prepared according to the procedures found in Portilla construction of complete cohort life tables. However, on the rate of and Streett (2006). increase and demographic parameters such as net maternity, there is little available information. Infante et al. (1993) and Portilla (1999a) Biological Parameters of C. stephanoderis and found that fecundity and survivorships were largely affected by the P. nasuta extremes of temperature; high mortality was found in immature Cohorts of 291 recently parasitized hosts by C.  stephanoderis and stages for C.  stephanoderis at 17°C, while at 37°C, all specimens 547 recently parasitized hosts by P. nasuta were used for this study. died. The longevity was inversely related to temperature, although The size of cohort depended on availability. Each cohort was divided fecundity rate was reduced (Portilla 1999b). into 13 subcohorts (replicates) and placed into rearing containers Studies conducted in Colombia demonstrated that CBB could be (20 and 40 parasitized hosts per container, respectively) (Pioneer controlled in commercial coffee farms using inoculative and inun- plastic 032C, Dixon, KY). They were held inside the environmental dative releases of the African parasistoid C.  stephanoderis, when chambers (16:8 [L:D] h photoperiod, temperature of 25°C, and 55% the infestation is lower than 5% (20 wasps every 2 mo per infested RH) and kept until the last adult was obtained. Parasitized hosts berry) (Salazar et al. 2002). Portilla (1999c) based on the results of were observed every day. Total number of parasitoids surviving from Salazar et al. (2002) assessed approximately how many wasps should egg through adult and adult emergence was recorded on a daily basis be used per releases by using a simulation model for improving eco- for each species. logical and economic recommendations for the control of the CBB in Twenty-five extra hosts recently parasitized by C.  stephanoderis Colombia (Developed by Adrian Leach funded by The Department and P. nasuta were individually placed into Petri dishes 25 × 11 mm for International Development, United Kingdom) (Portilla 1999c). (Thermo Fisher 121V) and observed daily to determine egg, larva, She gave the following example: The coffee harvest distribution of a prepupa, and pupa developmental time. From the 13 groups of each hectare of 5,000 coffee trees with approximately 1,500 ripe berries species, 15 copulated females were taken and individually confined per tree and 5% of CBB infestation would need about 4,400,000/ into larger Petri dishes (35 × 11 mm) that contained 30 CBB immature ha (20 wasps per infested berry) to keep the CBB population under stages (10 second-instar larvae, 10 prepupae, and10 pupae) for ovipo- the threshold (2% of infestation). These wasps would be distrib- sition as well as few eggs and first-instar larvae for feeding. The num- uted through the year with releases every 2 mo as follow: February ber of eggs oviposited every day by each parasitoid of both bethylids (260,000 wasps/ha), April (100,000 wasps/ha), June (480,000 wasps/ were counted and recorded until the last wasp was dead. Petri dishes ha), August (380,000 wasps/ha), October (2,000,000 wasps/ha), and were cleaned daily removing any dead or parasitized hosts and replac- December (1,200,000 wasps/ha). Producing those large numbers ing them with new ones. Means of number of eggs oviposited per each of parasitoids in a cost-effective way will depend on well-designed female, longevity, pre-post, reproductive, and reproductive periods of production facilities using industrial level mechanized and auto- C. stephanoderis and P. nasuta and their host preference for ovipos- mated rearing processes only. Portilla 1999a and Portilla and Streett iting were determined. The progeny of each female was maintained 2008 reviewed and discussed the requirements for a semiautoma- until adult emergence when sex ratio was determined. tion system for mass production of CBB and its African parasitoids including diet preparation, sanitation, environmental factors, qual- Demographic Parameter of C. stephanoderis and ity control, storage, and distribution. Unfortunately, no studies have P. nasuta examined calculation costs between the in vivo (naturally infested berries or parchment coffee methods) and the in vitro (artificial diet) Abridged life tables for both species of parasitoid were calculated rearing system for parasitoids production. However, to the best of according to Portilla et al. (2014). Immature survival was calculated our knowledge, no in vivo rearing system currently available will be using the subcohorts for each parasitoid species. The fraction of able to supply such demand. death was calculated by the sum of all dead in each developmental This study was conducted to obtain information on the bio- stage and divided for the total beginning stages (synthetic cohort). logical parameters and fertility rates of these parasitoid species in This value was used for incorporating in the adult survival parame- an effort to get a better understanding how to improve our ability to ter (l ). Data obtained for the number of parasitic females alive each rear large numbers for field release. Parasitoids were reared on CBB day at each age (x) and the number of eggs oviposited each day were using Cenibroca artificial diet. Abridged cohort life tables for both used to calculate the basic population parameters: gross maternity parasitoids were constructed for growth rate estimations. Results (M ), survival (L ), fecundity (m ), net maternity function (l .m ), x x x x x are presented with tables and figures with a detailed description net reproductive rate (R ), finite rate of increase (λ), intrinsic rate of all biological factors obtained by daily observations in life-table of increase (r ), mean generation time (T), and doubling time (DT) construction. (Krebs 2001, Pressat 1985, Carey 1993). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 3 parasitoids had a marked difference in survival between species for Statistical Analysis both eggs (F = 11.17; df = 1, 24; P = 0.0027) and pupae (F = 23.70; One-way analysis of variance and the Tukey’s Honest Significant df = 1, 24; P = 0.0001), while no differences in survival were observed Difference test (SAS Institute, 2013) were used to compare life-ta- for larvae (F = 4.21; df = 1, 24; P = 0.0512) (Table 2) . A comparison ble parameters, developmental time, preoviposition and oviposi- of female progeny production among species revealed that C. steph- tion period, longevity, immature mortality, and host preference. anoderis had a significantly higher reproduction than that of P.nasuta Nonparametric estimates of the survival function of females were (F = 15.95; df = 1, 28; P = 0.0004). There were significant differences compered between parasitoid species by using PROC LIFETEST test in female production per day (F = 151.85; df = 1, 940; P = 0.0001), procedure in SAS (SAS 2013). Regression analysis was used to deter- where C. stephanoderis female were found ovipositing 2.22 ± 0.06 mine differences in cumulative gross fecundity between C. stephan- (SE) eggs/day/female and P. nasuta 1.21 ± 0.06 (SE) eggs/day/female. oderis and P. nasuta. In general, both parasitods species were normally found ovipositing from one to three eggs per day. However, sporadic ovipositions from Results four to seven eggs per day were observed for C. stephanoderis and from four to five eggs per day for P.  nasuta. The number of eggs Biological Parameters of C. stephanoderis and per wasp varied from 38 to 114 eggs for C.  stephanoderis and 6 P. nasuta to 88 eggs for P.  nasuta. Suggesting that it could be related to the The percentages of host parasitized being offered equal numbers of amount of CBB stages provided during their entire life (about 300 second instar larvae, prepupae, and pupae of CBB of both parasi- CBB stages). Percentage of number of eggs oviposited per female toids are presented in Fig. 1. C. stephanoderis had high percentages among species is presented in Fig. 2. No C. stephanoderis population of parasitism in prepupae (60.85 ± 11.67 [SE]) followed by pupae was found with <20 eggs per wasp and 0% of P. nasuta population (36.61 ± 11.28 [SE]) and only small populations of parasitized sec- had >100 eggs per parasitoid. In total, 20% of C. stephanoderis and ond-stage larvae were observed (2.52 ± 1.77 [SE]), whereas P. nasuta 55% of P. nasuta population was found ovipositing 20–50 eggs per had a high preference for prepupae (50.29  ±  13.47 [SE]) followed female, while 53% of C. stephanoderis and 20 % of P. nasuta popu- by second-instar larvae (45.07 ± 14.72 [SE]) and occasionally par- lation was found ovipositing 50–100 eggs per female. asitized pupae were observed (4.63 ± 3.15 [SE]). There were signifi- Both parasitic wasps had a different behavior on host parasitisa- cant differences among preferences of parasitism percentage (df = 1, tion. C. stephanoderis oviposited a single egg per host and did not 28; P = < 0.0001; F = 123.33, 5.49, 79.15 for second-instar larvae, oviposit until the host was completely paralysed, whereas P. nasuta prepupae, and pupae, respectively). The developmental time to egg could oviposited more than one egg on host when they still moving, (F = 80.93; df = 1, 48; P = 0.0001), larvae (F = 11.19; df = 1, 48; although the host have had various stinging. This behavior could P  =  0.0016), and cocoon (F  =  32.05; df  =  1, 48; P  =  0.0001) was explain the statistic differences found on their pre-reproductive significantly different among species. There were no statistical dif- period (F = 16.56; df = 1, 28; P = 0.0003) and longevity (F = 7.55; ferences for prepupae (F = 0.05; df = 1, 48; P = 0.8295) and pupae (F  =  0.91; df  =  1, 48; P  =  0.3437) between parasitoids (Table  1). Cocoons were formed in 2 d for both parasitoid species. No Table  1. Mean developmental time for the immature stages of C. stephanoderis and P. nasuta developed on diet-reared CBB hosts cocoons were formed in 51.65% of C.  stephanoderis’s population and 42.46% of P.  nasuta, but individuals still developed to adult Life stages Developmental times (d) (Mean ± SE) maturity. The proportion of death in each immature stage of C. stephan- C. stephanoderis P. nasuta oderis and P. nasuta is presented in the Table 2. Using GLM analysis, Egg 3.00 ± 0.58a 4.48 ± 0.49b Larva 4.16 ± 0.84a 4.96 ± 0.63b Cocoon 3.84 ± 0.62a 2.84 ± 0.51b Prepupae 4.08 ± 0.65a 4.12 ± 0.53a Pupa 13.60 ± 1.03a 13.32 ± 0.85a Total time to adult 28.68 ± 1.58a 29.72 ± 1.05b Means ± SE followed by the same letter in each row are not significantly different (P < 0.05, Tukey’s test) (N = 25 per species). Table  2. Immature stage mortality for C.  stephanoderis and P. nasuta developed on diet-reared CBB hosts Stages/parameters Percentage immature mortality (mean ± SE) C. stephanoderis P. nasuta Eggs 4.17 ± 4.08a 12.33 ± 7.10b Larvae 11.09 ± 6.31a 17.93 ± 9.74a Pupae 1.4 ± 1.89a 12.61 ± 7.53b Cumulative mortality 16.12 ± 6.98a 36.31 ± 14.66b Survival to adulhood 83.87 ± 6.42a 63.69 ± 15.08b Fig.  1. Hosts preference percentage parasitized by C.  stephanoderis and P.  nasuta. Bars not sharing the same uppercase letter are significantly Means + SE followed by the same letter in each row are not significantly different. (Tukey’s test P = 0.05) (means ± SE). different (P < 0.05, Tukey’s test). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2018, Vol. 18, No. 2 df = 1, 28; P = 0.0104). Preoviposition period (17.26 ± 10.57 d) and X  = 11.10, df = 1, P < 0.0009) (Fig. 3B). Differences in the cumu- longevity (63.13 ± 13.23 d) were significantly longer for P.  nasuta lative gross fecundity, indicating a logarithmic regression type with as compared to C.  stephanoderis, (4.25 ± 0.43 and 46.66 ± 15.41 r values of 0.997 and 0.979 for C.  stephanoderis and P.  nasuta, d). GLM showed no significant differences among parasitoids on respectively, is illustrated in Fig. 3C. reproductive (F = 0.83; df = 1, 28; P = 0.3706) and postreproductive Seven life-table parameters are presented in Table 5. The higher periods (F = 3.98; df = 1, 28; P = 0.0559) (Table 3). During their pos- gross fecundity occurred for C.  stephanoderis with 73.06  ±  26.22 treproductive period both wasp species continued feeding upon their (SE) eggs per wasp, while 35.93  ±  24.68 (SE) eggs per wasp was hosts. Both parasitoid species tended to produce more females than obtained to P. nasuta. Finite rate of increase (λ) is the factor by which males, but their sex ratio varied among species. Total eggs deposited a population increases each day and is determined by the intrinsic by C. stephanoderis and P. nasuta and sex ratio among paratitoids rate of increase (r ). C. stephanoderis had the highest finite rate of are presented in Table 4. increase. The growth rate per generation of C.  stephanoderis was 46.15 female wasps per newborn female with a mean time of 47.39 d. The daily growth rate was 1.09 daughter females per female, dou- Life-Table Parameter of C. stephanoderis and bling this number in 6.5 d. The growth generation for P. nasuta was P. nasuta 18.33 daughter females per female with a mean time of 58.60 d; its Life-table data indicated differences between the two parasitoid spe- daily growth rate was 1.05 females per female doubling this number cies. For example, mean daily egg production (M ) for C. stephanod- in 13.12 d. eris increased to almost 4.0-fold during the first week and remained at high numbers of egg production until the end of the second week (Fig.  3A). Subsequently, the production of this parasitoid declined Discussion over the next 5- to 6-wk period reaching zero by about day 50. The parasitic wasps C.  stephanoderis and P.  nasuta are idiobionts Alternatively, P. nasuta showed a constant trend in production from ectoparasitoids that attack every stage of CBB ovipositing on final- day 19 to day 45. Mortality, analyzed by the test of equality with stage larvae (2.52 and 45.07%), prepupal (60.85 and 50.29%), and the strata statement in –log (survival probability) PROC LIFETEST, the pupal stages (36.61 and 4.63%), respectively, which is quite indicated significant differences among parasitoids (Log-Rank common among idiobiont ectoparasitoids (Shaw 1994). Both par- asitoids preferred to feed on pupae rather than eggs or early instar larvae. The percentages of host preference obtained in this work differ from Barrera et  al. (1989) and Abraham et  al. (1990) who found that C.  stephanoderis preferred ovipositing on pupae rather than prepupae. However, Infante (1993) observed 55.4% of eggs on prepupae and 44.6% on pupae. Portilla (1999) found similar results for C. stephanoderis, which was exposed to different temperatures . Lateral-abdominal oviposition occurring only on prepupa has been reported for P. nasuta by Waterson (1923); Hargreaves (1926, 1935); Puzzi (1939); Toledo (1942); Abraham et  al. (1990); and Murphy and Rangi (1991). Oviposition was never seen on prepupa except by Toledo (1942). In this study, P. nasuta was found ovipositing eggs on the dorso-abdominal of the pupa and in a variety of areas on both prepupa and second-instar larval of CBB. There are two general forms of the life table, using original or hypothetical cohorts (Carey 1993). The first is the cohort life table, which provides a longitudinal perspective that includes the mortality experience of a particular cohort from the moment of birth through consecutive ages until no individuals remain in the original cohort. The second is the abridged life table, which assumes a hypothetical Fig. 2. Population percentage of C. stephanoderis and P. nasuta oviposition cohort subject throughout its lifetime to the age-specific mortality number of eggs per female (n = 15 parasitoid females). rates prevailing for the actual population over a specific period. Most aspects of the life history of C.  stephanoderis and P.  nasuta Table  3. Preoviposition, oviposition, and postoviposition periods, have been collected from studies carried out in captivity using a and longevity of C. stephanoderis and P. nasuta developed on diet- reared CBB hosts Table  4. Total production and sex ratio of C.  stephanoderis and Periods Developmental (Means + SE) P. nasuta developed on diet-reared CBB hosts times (d) Variable Parasitoids C. stephanoderis P. nasuta C. stephanoderis P. nasuta Preoviposition 4.53 ± 0.43a 17.26 ± 10.57b Oviposition 32.13 ± 13.16a 28.40 ± 8.42a Total eggs oviposited 1,101 540 Postoviposition 11.00 ± 8.54a 17.46 ± 8.58a Total adult emerged 815 388 Adult longevity 47.66 ± 15.41a 63.13 ± 13.23b Total females 702 302 Total males 113 86 Means ± SE followed by the same letter in each row are not significantly Sex ratio 6.2:1 3.5:1 different (P = 0.05, Tukey’s test) (N = 15 per species). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 5 Table  5. Life-table statistic for C.  stephanoderis and P.  nasuta reared on H. hampei developed on diet-reared CBB hosts Parameters and units Parasotoids C. stephanoderis P. nasuta Gross fecundity (M ) 81.32 39.44 Fecundity (m ) 67.99 31.09 Net reproductive rate (R ) 46.15 18.33 Mean generation time (T) 47.39 58.60 Doubling time (DT) 7.78 13.12 Intrinsic rate of increase 0.089 0.052 Finite rate of increase (λ) 1.09 1.05 Total offspring/female. Females/female at age x. Daughters/new-born female (Population which increases each generation). Mean age of reproduction (d). Time required for (λ) to doubling number. Rate of natural increase (daughters/female/day). Individuals/female/day. for preoviposition and 30.6 d from egg to adult at 27ºC and 75% RH. At 25ºC and 90% RH, Abraham, et al. (1990) obtained a pre- oviposition period of 14 d and development time of 22.4 d at 25°C. The statistical analysis of the synthetic cohort used for C. steph- anoderis and P. nasuta permitted the construction of abridged life-ta- ble functions, which were computed daily over their entire life. The development time from egg to adult did not vary appreciably from results obtained by different researchers with temperatures of 25°C. P.  nasuta had a higher mortality value for every immature stage in comparison to C.  stephanoderis (Table  2). The low mortality of C. stephanoderis is probably reflected in the ability of the female to select high-quality hosts (large and healthy) for oviposition, whereas P. nasuta was observed ovipositing eggs on larvae when the paraly- sis process was uncompleted. The capacity of predation of P. nasuta is another characteristic that impacts mortality, due to the female ovipositing eggs on the host where predation was initiated and even oviposited on small larvae. In effect, this type of stage selection does not provide all the resources necessary for its survival. These behav- ioral characteristics for P. nasuta provide a better understanding why this parasitoid has been difficult to rear under laboratory conditions. Portilla (1999a) reported only 28.4 stages per parchment coffee at 25 d after infestation, and from this population only a 29.09% has the probability to be parasitized by C. stephanoderis. This percentage Fig.  3. Life-table data of C.  stephanoderis and P.  nasuta restricted to adult would be lower if the same population was parasitized by P. nasuta. stage. (A) gross fecundity (Mx); (B) survival (lx); and (C) regression of In captivity, and under good conditions, many wasp species will cumulative gross fecundity. live 1 or 2 mo (Quicke 1997) . Barrera et al. (1989) investigated the effect of adult diet on longevity of C.  stephanoderis. He mentioned hypothetical cohort. This is because under normal circumstances, its that longer longevity was found (77 d) when the adults were procided complete life cycle is not feasible. Several studies have reported com- a honey–water mixture. However, Murphy and Rangi (1991) reported parative data for different feeding regimes, temperatures, and some only 2 d for P. nasuta when fed honey and there were no significant aspects of oviposition behavior and reproductive potential. Koch differences when fed CBB pupas and adults with no additional food. (1973) showed that C.  stephanoderis has a developmental time of The same authors reported 14 d when P. nasuta was fed CBB eggs and 23.2, 20.0, 15.2, and 14.6 d at 24, 27, 30, and 32°C, respectively. larvae. The larger longevity of C. stephanoderis and P. nasuta found Also, the preoviposition time varied from 8.0 d at 21°C to 2.0 d in this study could be related to the amount of suitable hosts pro- at 27°C. However, 10 d at 17°C and 2 d at 32°C was the preovi- vided during their entire life (almost 300 CBB stages per female wasp). position period identified by Infante (1993). Portilla (1999) found Fecundity ranges enormously in parasitic wasps and depends upon that the preoviposition period occurred in 4.5 d at 23°C, 3.7, 2.9 several factors, including species, size, and diet (Jervis and Copland and 2.1 d at 25, 27, and 29°C, respectively. She also reported devel- 1996). Abraham et  al. (1990) found that female C.  stephanoderis opmental times of 28.1, 25.1, 23.2, and 19.9 d at 23, 25, 27, and could lay 1–3 eggs and occasionally 4 per day and produce up to 70 29°C, respectively. Eggs hatch varied from 4.1 d at 23°C to 2.9 d at eggs during her life. Barrera et al. (1989) found up to 9 eggs per para- 29°C, Abraham et al. 1990 found that at 25ºC eggs hatched in 1.61 sitoid per day and the most fecund individual produced 139 eggs in 66 d. Murphy and Rangi (1991) reported that P.  nasuta needed 5.3 d Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Journal of Insect Science, 2018, Vol. 18, No. 2 d. In this study, the numbers of eggs per C. stephanoderis varied from Aristizabal, L. F. and A. E. Bustillo, S. P. Arthurs. 2016. Integrated pest man- agement of coffee berry borer: strategies from Latin American that could 34 to 114, and from 6 to 88 to P. nasuta. C. stephanoderis, on average, be useful for coffee farmers in Hawaii. Insects. 7:1–24. oviposited 81 eggs per wasp in 47.6 d and in comparison, P. nasuta Baker, P. 1999. La broca del café en Colombia: informe final del proyecto MIP oviposited 47 eggs in 63.1 d.  These results indicate that under field para el café DFID—Cenicafe. CABI Bioscience, Ascot, United Kingdom. conditions, females of C.  stephanoderis and P.  nasuta never obtain enough hosts to achieve full reproductive potential. Several studies Barrera, J. F., A.  Castillo, F.  Infante, J.  Gómez, and W.  De La Rosa. 1989. confirmed that females always predominate in these two bethilides. Biologie de C. Stephanoderis (Betrem) (Himenóptera: Bethylidae) en lab- The field sex ratio of the parasitic wasp C. stephanoderis recorded by oratorio. Cicle bioloque, capasite de oviposition, et emergente du fruit du Ticheler (1961) was 4.8 females per 1 male, and Koch (1973) found cafeier. Café Cacao, The Francia. 33: 101–108. 2.7 females per 1 male. Barrera et al. (1993) obtained a sex ratio of 7:1 Benassi, V. L. 1995. Levantamiento dos inimigos naturais da broca du café under laboratory condition, while Benassi (1998) found a P nasuta a Hypothenemus hampei (Coleoptera: Scolytidae) no norte du Espiritu Santo. An. Soc. Entomol. 24: 635–638. sex ratio of 5.2 females per male. This ratio varied through various Bustillo, A., J. Orozco, P. Benavides, and M. Portilla. 1996. Producción masiva generations, with 28.5 females per male after five generations. The sex y uso de parasitoides para el control de la broca del café en Colombia. Rev. ratio obtained in this work was 6.2: 1 and 3.5: 1 for C. stephanoderis Col. Entomol. 47: 215–230. and P. nasuta, respectively. Carey, J. R. 1993. Applied demography for biologist with special emphasis on According to these results C.  stephanoderis produced more insects. Oxford University Press, Oxford, United Kingdom, p. 206. females per female than P. nasuta (R ), but both parasitoids need at Carey, J. R., T. Y. Wong, and M. M. Ramadan. 1988. Demographic framework less 50 suitable host stages to assure progeny. The speed at which the for parasitoid mass rearing: case study of Biosteres tryony (Hymenoptera: colony increased (r ) is the most important parameter, and C. steph- Braconidae), a larval parasitoid of tephritid fruit flies. Theor. Popul. Biol. anoderis obtained a high intrinsic rate of increase. Mass production 34: 279–296. of both parasitoids depends on the host reproductive potential, and Hargreaves, H. 1926. Notes on the Coffee berry bore. Bull. Entomol. Res. 16: 347–354. hence, these results provide insight as to why the parasitoids have Hargreaves, H., 1935. Stephanoderis hampei Ferr. Coffee berry borer in been so unsuccessful in the field, because to proliferate they evidently Uganda. East Afri. Agric. 1:218–224. need a range of host stages. If a wasp attacks an immature berry, it Infante, F. and L. J. Barrera. 1993. Estadísticos demográficos de Cephalonomia will encountered only eggs and young larvae which they may con- stephanoderis Betrem (Himenóptera: Bethylidae) a temperaturas con- sume and kill the CBB female as well, but the female parasitoid will stantes. Folia. Entomol. Mex. 87: 61–72. not produce any offspring (Baker 1999, Ruiz-Cardenas and Baker Infante, F., L. J. Barrera, J. Gomez, and A. Castillo. 1992. Thermal constants 2010). In addition, if the wasp arrives too late, they will find mostly for pre-marginal development of the parasitoid Cephalonomia stephanod- adult CBB and have to wait until they start breeding, by which time eris Betrem (Hymenoptera: Bethylidae). Can. Ent. 124: 935–941. harvest may intervene. All this suggests that C.  stephanoderis and Infante, F., J. Valdes, V. Penagos, and J. Barrera. 1994. Description of the life P. nasuta will be incompatible with efficient commercial production. stages of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), a par- asitoid of Hypothenemus hampei (Coleoptera: Scolytidae). Vedalia. 1: However, we must consider studies that have demonstrated that a 13–18. high number of wasps per hectare (20 wasps per infested berry every Jervis, M. A. and M. J.  Copland. 1996. The life cycle. In: M. A. Jervis and 6 mo) can control CBB or keep it under controls in plots with less N. Kidd (ed.), Insect natural enemies. Chapman and Hall, London. than 5% of CBB infestation (Aristizabal et  al. 1997, Salazar and pp. 63–161. Baker 2002, Aristizabal et al. 2011). Krebs, C. J. 2001. Ecology: the experimental analysis of distribution and abun- dance, 5th ed. Wesley Longman, San Francisco, CA. p. 695. Kock, V. J. 1973. Abondance de Hypothenemus hampei Ferr. Scolyte des graines Acknowledgments de café en function de sa plante hote et de son parasite Cephalonomia The authors would like to thank Luis Carlos Jojoa former technician at USDA, stephanoderis Betrem en Cote de’ Ivore. Medd. Landbou. 73: 1–85. ARS, BCPRU, Starkville, for their valuable support in rearing the host and par- Murphy, S. and D. Moore. 1990. Biological control of the coffee berry borer, asitoid colonies. We are also grateful to Carlos Blanco (SIMRU-ARS-USDA) Hypothenemus hampei (Ferrari) (Coleoptera, Scolytidae): previous pro- and Arnubio Valencia (Nebraska University, Department of Entomology) for grams and possibilities for the future. Biol. Control. 11: 107–117. critically reviewing an early version of this manuscript. Murphy, S. T. and D. K. Rangi. 1991. The use of the African wasp, Prorops nasuta for the control of the Coffee Berry Borer, Hypothenemus hampei in Mexico and Ecuador: the Introduction program. Insect. Sci. Applic. 12: References Cited 27–34. Abraham, Y. J., D. Moore, and G. Godwin. 1990. Rearing and aspects of biol- Portilla, M. 1999a. Mass rearing technique for Cephalonomia stephanod- ogy of Cephalonomia stephanoderis and Prorops nasuta (Hymenoptera: eris (Hymenoptera: Bethylidae) on Hypothenemus hampei (Coleoptera Bethylidae) parasitoids of the coffee berry borer, Hypothenemus hampei Scolytidae) developed using Cenibroca artificial diet. Rev. Col. Entomol. (Coleoptera: Scolytidae). Bull. Entomol. Res. 80:121–128. 25: 57–66. Aristizabal, L. F., P. S.  Baker, J.  Orozco, and B.  Chavez. 1997. Parasitismo Portilla, M. 1999b. Desarrollo y evaluación de una dieta artificial para la de Cephalonomia stephanoderis (Betrem) sobre una poblacion the cría masiva de Hypothenemus hampei (Coleoptera: Scolytidae). Rev. Col. Hypothenemus hampei (Ferrari) con niveles bajos de infestacion en Entomol. 1: 24–38. campo. Rev. Colomb. Entomol. 23:157–164. Portilla, M. 1999c. Mass production of Cephalonomia stephanoderis on Aristizabal, L. F., P. S. Baker, J. Orozco, and B. Chavez. 1998. Effecto del para- Hypothenemus hampei reared using artificial diet. Thesis. Univerisity of sitoide Cephalonomia stephanoderis (Hymenoptera: Bethylidae) sobre las London, England. 253 pp. poblaciones de Hypothenemus hampei (Coleoptera: Scolytidae) durante y Portilla, M. and A. Bustillo. 1995. Nuevas investigaciones en la cría masiva de despues de la cosecha. Rev. Colomb. Entomol. 24:149–155. Hypothenemus hampei y de sus parasitoides Cephalonomia stephanoderis Aristizabal, L. F., M.  Jimenez, A. E.  Bustillo, and S. P.  Arthurs. 2011. y Prorops nasuta. Rev. Col. Entomol. 21: 25–33. Introduction of parasitoids of Hypothenemus hampei (Coleoptera: Portilla, M. and D.  Streett. 2006. Nuevas técnicas de producción masiva de Scolytidae) on small coffee plantations in Colombia through farmer par- Hypothenemus hampei sobre la dieta artificial Cenibroca modificada. Rev. ticipatory methods development. Fla. Entomol. 94: 690–693. Col. Entomol. 57: 37–50 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 7 Portilla, M. and D.  Streett. 2008. Avances investigativos en la produc- Salazar, H. M. and P. Baker. 2002. Impacto de liberaciones de Cephalonomia ción masiva automatizada de la broca del café Hypothenemus hampei stephanoderis sobre poblaciones de Hypothenemus hampei. Rev. Col. (Coleoptera: Scolytidae) y de sus parasitoides sobre dietas artificiales. Sis. Entomol. 53: 306–316. Agroeco. Mod. Biomatematics. 1:9–12 SAS Institute. 2013. SAS/STAT user’s manual, version 9, 4th ed. SAS Institute, Portilla, M., J.  Ramos-Morales, G.  Rojas, and C.  Blanco. 2014. Life tables Cary, NC. as tools of evaluation and quality control for arthropods mas produc- Shaw, M. 1994. Parasitoid host range. In: B.A. Hanwkins and W. Sheeham tion. In: J. Morales-Ramos (ed.) 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K., C. Simi, K. Tintumol, and P. K. Vinodkumar. 2014. Life Ruiz-Cardenas, R. and P.  Baker. 2010. Life table of Hypothenemus hampei cycle of the coffee berry borer parasitoid, Cephanolomia stephanoderis (Ferrari) in relation to coffee berry phenology under Colombian field con- (Hymenoptera: Bethylidae) on parchment and cherry coffee. Int. J. of Sci. ditions. Sci. Agric. 67: 658–668. Tech. Research. 3: 151–152. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/20/4916095 by Ed 'DeepDyve' Gillespie user on 16 March 2018

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