Effects of Pichia kudriavzevii on development, larval mortality and adult fecundity of Zaprionus indianus (Diptera: Drosophilidae) at different temperatures.

doi:10.21203/rs.3.rs-2734977/v1

Host–pathogens interactions are sensitive to changes in temperature. Increase in temperature significantly influences the distribution of fruit flies. African fig fly, known as Zaprionus indianus (Gupta) (Diptera: Drosophilidae) is one of the invasive, secondary insect pests of fruits. The current article explores the effect of temperature and fungal infection on Z. indianus life history traits. Development of Z. indianus was observed on locally isolated fungus Pichia kudriavzevii (Boidin, Pignal and Besson, 1965) (Saccharomycetales: Pichiaceae) treated and untreated medium. Pre- adult and adult life stages of treated and untreated individuals at different temperatures showed significant difference in trait values and mortality. At extreme temperatures (i.e. 17◦C and 31◦C) the life history traits (egg hatchability, viability, adult emergence, pupation rate and fecundity) in fungi- treated food showed significant reduction in trait values except in development period (egg to adult stage) at 17◦C. High temperatures (28◦C and 31◦C) favour shorter fungal development period but that of Z. indianus was considerably delayed by 5 days at all tested temperatures in treated medium. The current work illustrates the consequences of temperature and fungal infection on the developmental stages and physiological traits of Z. indianus. The combination of the biotic and abiotic factors aids in understanding of the response of pest species of Drosophila to differential temperature ranges and fungal infection; hence, the present study could assist in predicting the driving ecological factors that mediate the containment of Z. indianus, an invasive secondary pest of India.

Drosophila

Pichia kudriavezvii

Zaprionus indianus

thermal stress

life history traits

ecology

The ecology and consequently the survivability of ectothermic organisms are considerably intimidated by the temperature due to the direct effect on the biochemical processes of an organism (Viña 2002) and as a result invasive populations of various species have to thrive under extreme conditions of new demographic niches (Merino et al. 2019). Zaprionus indianus (Gupta) (Diptera: Drosophilidae) is a semi-cosmopolitan species which originated from Afrotropical region, mostly feeding on figs and hence, gained its name as African fig fly. It has invaded over several continents, including India in the 1970s, making it the most ecologically adapted drosophilid species ranging from tropical to subtropical regions (Commar et al. 2012; Eppo Alert 2020). Since distribution of species is greatly influenced by temperature, species of invasive populations have to commit to trade-offs such as genetic diversity loss probably harmful for their fitness (Comeault et al. 2020). Besides this, invasive population face various biological challenges such as introduction to microbial pathogens. The physiology and behaviour of insects is directly or indirectly affected by the microbial infections and temperature which have repercussions in ecological interactions like predation influencing the population dynamics (Cory and Ericsson 2010). Generally, immune system of the insect host plays vital role in defence against microbial pathogen but they respond to natural infections in a variety of other ways as well. Non-immunological defences such as behavioural modifications and physiological adaptations in response to microbial pathogens are often the most neglected area of research related to patho-physiological studies with insects (De Roode and Lefèvre 2012; Parker et al. 2011). A slight change in temperature not only affects fruit fly population but microorganisms too including fungi which are sensitive to temperature extremities contributing substantially towards the geographic range expansion of known fungal pathogens (Gadre et al. 2022; Sautour et al. 2001). All pathogenic microorganisms have well-studied temperature ranges between 15◦C and 37◦C, and can better survive up to 40◦C with pH tolerance ranging from 5.4 to 7.4 (Casagrande Pierantoni et al. 2021; Nadeem et al. 2013). As a result, extreme temperature change may elicit the emergence of hitherto harmless or unrecognised fungal species. Hence, with an eye toward the understanding of implications of the temperature and microbial stressors on Z. indianus, it is important to elucidate the host-pathogen interaction from an ecological point of view.

Control of invasive pest population of fruit flies was mainly through chemicals but proved to be ineffective and quite expensive encouraging further research for alternate management techniques. One of the indispensible measure to control insect pests is to identify strategies stemmed from the temperature-dependent physiological responses as it directly influences insect physiology including behaviour, metabolic processes and lifespan (Sharpe and DeMichele 1977). Moreover, identification of natural antagonists including microbial pathogens and parasites may facilitate the development of effective biological control of fruit fly pest (Marchiori & Silva 2003). In the present study, effect of temperature (17◦C, 21◦C, 25◦C, 28◦C, 31◦C) on the developmental traits of Z. indianus was studied under the influence of locally isolated fungus and uninfected control in order to address the following questions: (i) how different temperatures independently affect fungal growth and Z. indianus development?, (ii) what is the impact of fungal infection and diverse temperature ranges on the development and life history of pest species of Drosophila, Z. indianus?

2.1. Insect Collection and Rearing

Wild Zaprionus indianus were collected for experimental purpose from three geographical regions of Northern India: Punjab (31°04′18.48″ North, 75°24′16.92″ East and 150m to 551m), Solan (30°54'16.15" North, 77°5'48.25" East, 1451.96 m) and Shimla (31°6'17.33" North, 77°10'24.25" East and 2196.88 m) using guava baits. Cadavers of Z. indianus killed by fungi within baits were collected and bought under laboratory conditions. All wild caught flies were maintained at 25°C, 60% Relative humidity (RH) with a 12 h/12 h light/dark cycle on standard Drosophila medium containing cornmeal-sugar-agar in fixed proportions.

2.2. Isolation and Identification of Fungi

Fungi from dead cadavers were cultured using method of Hajek et al. (2012a) in Potato Dextrose Agar (PDA) medium (HiMedia Laboratories, Maharashtra) at 25°C. The fungal colonies were allowed to grow at the optimal temperature of 28°C − 30°C for 48 h of incubation. The fungal strain was isolated by sub-culturing in order to obtain single isolated colony which was examined morphologically and microscopically. The fungal isolate was identified by the highest similarity of ITS1 and ITS2 region sequences to known strains from National Centre for Biotechnology Information (NCBI) Blast search. The sequencing result was submitted to the GenBank (NCBI) in order to obtain the accession number.

2.3. Preparation of Fungal suspension

Fungi isolated from Z. indianus were used for preparing fungal suspension by the method of (Sangbaramou et al. 2018). The liquid fungal suspensions were prepared from 7 days old cultures of fungus by adding 20 ml sterile distilled water and scraping off the culture using the sterile glass slide. The extracted aqueous suspension was homogenized by adding 0.1% Tween 80 as an emulsifier under magnetic stirring until the PDA got removed from the fungal biomass, which was then filtered through syringe or sterile filter paper. The fungal cell count was adjusted counted to 10⁷ cells/ml using haemocytometer. The fungal suspension can be stored for long term usage at 4◦C by adding 7.5% of glycerol (Guijarro et al. 2007).

2.4. Fungal Growth rate at different temperatures

For the evaluating the fungal growth rate, fungal plug of 6–7 day old culture (5 mm in diameter) was centrally inoculated onto plates containing standard Drosophila medium in order to maintain the same growth conditions as for the development of Z. indianus. The plates were incubated at 17◦C, 21◦C, 25◦C, 28◦C and 31◦C for 5–6 days. Fungal growth rate was assessed daily by calculating the diameter of the spreading colonies in millimeter (mm) (Patriarca et al. 2001). Radial growth of fungal colonies was plotted against time as mm/ day (Yunes et al. 2020). The experiments were performed in quadruplicate.

2.5. Impact of temperature on development time of Z. indianus

A temperature range of 17◦C, 21◦C, 25◦C, 28◦C, 31◦C at 80 ± 2.5% RH were tested for the development of Z. indianus, based upon the geographical locations of isolation of fungi with the insect host. Development time (DT) taken to complete the egg to adult stage was recorded at respective temperatures within the experimental vials (25 × 100 mm Polystyrene vials) using the formula:

$$\text{D}\text{T} =\frac{{\Sigma }\text{n}\text{d} \text{*} \text{d}}{{\Sigma }\text{n}\text{d}}$$

1

,

where n_d is the number of flies emerging in d days after the eggs were laid.

2.6. Impact of temperature and fungi on the life history traits of Z. indianus

The impact of temperature and fungal infection on the developmental traits of Z. indianus was tested in the laboratory. Treated food within the experimental vials contained fungal spores (10⁷ cells/ml) while untreated food without the fungal cells served as the control. Around 30 pairs of flies per replicate were allowed to lay eggs on normal food substrate within the petri-dishes (90 mm × 15 mm) for 1–2 days, which were then removed after sufficient egg-laying. Around 50 eggs were collected from the petri dishes and transferred into the treated and untreated food substrate within the experimental vials and incubated at different temperatures (17◦C, 21◦C, 25◦C, 28◦C, 31◦C) at 80 ± 2.5% RH. The adult eclosion was recorded every 24 h till for 72 h till no eclosion within the vials. Per cent egg viability was calculated per vial as the percentage of individuals that emerged from the 50 eggs, while, percent egg hatchability was estimated per vial as the percentage of eggs hatched to 1st Instar larvae from those 50 eggs placed on the surface of the treated and untreated food. Percent adult emergence was calculated per vial as the percentage of individuals emerged as adults from 50 eggs, while and development time was calculated using the formula (1) in all the experimental units. All temperatures and fungal treatments were performed in triplicates.

2.7. Impact of temperature and fungi on the Fecundity of Z. indianus

Fifteen-twenty virgin (7–8 days old) females of Z. indianus were exposed to 5–7 day old culture of fungus (~ 0.1 × 10⁶ cells/mL) for 6–7 hours and then placed in normal food. An equal number of untreated male flies were added to each vial containing 10 pair each for 12 hours. After the mating, female flies were transferred to normal food vials for 24 hours and number of eggs laid per fly per day were counted for each fungal treatment (Dimbi et al. 2013). Control female flies having fed normal food was run in parallel. Each treatment was performed in triplicate.

2.8. Statistical analysis

Influence of temperature and fungal infection on development of Z. indianus were analysed by two-way analysis of variance (ANOVA) by subjecting data in Minitab 17. The differences among mean values were ranked by the Tukey’s HSD Test (p < 0.05). All treatments were performed in triplicates.

3.1. Isolation and identification of fungi

Wild Z. indianus collected from three geographical locations was evaluated for fungal colonies. Maximum association frequency of fungus was that of P. kudriavzevii (Boidin, Pignal and Besson 1965) (Saccharomycetales: Pichiaceae) which belonged to the division Ascomycota and found from Chandigarh population (98.5%), followed by Solan (15.5%) and Shimla (0.6%). The identified fungal strain was assigned the GenBank accession no. OP602996 and isolate zibd3. The proportion of P. kudriavzevii isolate zibd3 (p < 0.001***) was higher in Z. indianus from Chandigarh population and hence, further explored at different temperatures (Table 1). Fungal association on the surface of adult Z. indianus was irrespective of the gender of the fly.

Table 1

Average temperature (T_ave± S.E.) of three biogeographical locations from which wild *Z. indianus* was collected and the associated fungal frequency (%± S.E.).
Location	T_ave (◦C)	Z. indianus Collected	P. kudriavzevii Association Frequency (%)
Chandigarh	31.1	14.8 ± 18	98.5 ± 1.5
Solan	21.3	10.5 ± 15	0.5 ± 1.2
Shimla	17.6	4.2 ± 8	0

3.2. Impact of temperature on development of fungus

Figure 1 (a.) shows the growth rate of the P. kudriavzevii zibd3 on standard Drosophila medium as a function of different temperatures (17°C, 21°C, 25°C, 28°C, and 31°C). The results indicated that fungal growth took 2–3 days for fully covering the lawn of experimental plates at higher temperatures (28◦C, 31◦C) serving as optimum for its growth, while lower temperature ranges (17◦C, 21◦C) delayed development time by 3 days. At 25◦C, fungal growth took 4 days for full development [Figure 1 (b.)] with an average growth rate of 3–4 mm/day at higher temperatures (25◦C, 28◦C, 31◦C) and 0.5-1 mm/day at the lowest temperature (17◦C).

3.3. Impact of temperature on development of Z. indianus

Development time (egg to adult stage) of Z. indianus was evaluated independently on untreated food at different temperatures (17◦C, 21◦C, 25◦C, 28◦C, 31◦C). Lower temperature favoured longer development time by 29.77 days on an average while at extreme higher temperature (31◦C) took around 11 days to complete its development cycle from egg to adult stage as shown in Fig. 1 (b.). Hence, independently, temperature could significantly affect total development period of Z. indianus (f _{(4, 290)} = 2471.16, p < 0.05*).

3.4. Impact of temperature and fungus on life history traits of Z. indianus

3.4.1. Total development period of Z. indianus

Development period of Z. indianus was tested on fungal treated food at four different temperatures (17◦C, 21◦C, 25◦C, 28◦C, 31◦C). At highest tested temperature (31◦C), the total developmental period of Z. indianus was incomplete as no individual emerged from egg to adult stage. However, at lower tested temperatures (21◦C, 25◦C, 28◦C), development period was significantly increased (p < 0.001). At the lowest tested temperature (17◦C), as the fungal growth was delayed, development time of Z. indianus was not significantly affected as it was delayed by 1.5 days. Hence, impact of fungal growth was found insignificant at lowest temperature (17◦C) and considerably affected at extreme higher temperature (31◦C) as shown in Fig. 1 (c.). Fungal treatment independently affected the development period of Z. indianus (f _{(4, 290)} = 645.77, p < 0.0001***). However, combined effect of temperature and fungus was also quite significant against the Z. indianus development time (f _{(4, 290)} = 574.27, p < 0.001**).

3.4.2. Egg hatchability and viability

Egg hatchability and viability considerably decreased at higher temperatures from 21◦C to 31◦C, while at lowest tested temperature (17^◦C), egg hatchability was only 20% [Figure 2 (a.)] and viability was 15.8% [Figure 2 (b.)] in fungal treated food as compared to untreated food. Independent effect of fungal treatment on egg viability was quite significant (f _{(4, 290)} = 54228.33, p < 0.0001***) as compared to temperature (f _{(4, 290)} = 606.56, p < 0.005*). However, combined effect of temperature and fungal treatment was also quite significant (f _{(4, 290)} = 1147.93, p < 0.001**) compared to the temperature alone. Similarly, egg hatchability was significantly affected due to fungal treatment (f _{(4, 290)} = 77999.48, p < 0.0001***) compared to the temperature effect alone (f _{(4, 290)} = 231.35, p < 0.005*), while the trait was also considerably affected under dual effect of temperature and fungal treatment (f _{(4, 290)} = 1400.14, p < 0.001**).

3.4.3. Adult emergence of Z. indianus

Adult emergence of Z. indianus was lowest at extreme temperatures tested (17◦C and 31◦C) in the presence of fungal treated food. Results demonstrated that at 21◦C maximum adults were emerged (23 ± 2.1) in treated food as compared to other temperatures. However, the lowest adult emergence rate was observed at 31◦C in fungal inoculated food (11 ± 1.5) as shown in Fig. 2 (c.). Hence, fungal treatment significantly affected adult emergence with f _{(4, 290)} = 17142.55 (p < 0.0001***) as compared to temperature (f _{(4, 290)} = 154.35, p < 0.005*) alone. However, combined effect of temperature and fungal was also significant (f _{(4, 290)} = 268.22, p < 0.001**) as compared to the untreated control.

3.4.4. Fecundity of Z. indianus

Number of eggs laid by an adult Z. indianus female per day was significantly affected at all tested temperatures after 6–7 hours exposure with the fungal treated food. At highest temperature (31◦C) and lowest temperature (17◦C), only 1–3 eggs were laid, while the maximum egg laying was observed at 21◦ and 25◦C with 8.4 to 9 eggs laid per female per day [Figure 2 (d.)]. Hence, fungal treatment significantly affected fecundity of Z. indianus with f _{(4, 290)} = 8515.24 (p < 0.0001***) as compared to temperature (f _{(4, 290)} = 710.74, p < 0.005*) and combined effect of temperature and fungal treatment (f _{(4, 290)} = 730.88, p < 0.005*).

The results of two-way ANOVA are summarized in Table 2.

Table 2

Results of Two-way ANOVA applied to test the effect of fungal treatment and temperature on life history attributes of *Z. indianus*
Trait				Treatment			Treatment × Temperature	P value
	(df)		(1)		(4)		(4)	-
Development time (days)		F-value		645.77		2471.16	574.27	0.050061
Egg Viability (%)		F-value		54228.33		606.56	1147.93	0.000047
Egg Hatchability (%)		F-value		77999.48		231.35	1400.14	0.000001
Fecundity (N)		F-value		8515.24		710.74	730.88	0.008817
Adult emergence (%)		F-value		17142.55		154.35	268.22	0.000109

(df) = degree of freedom, p value (α level) = 0.05.

In the present paper we examined how different temperatures critically affect the interaction between a host (Z. indianus) and its native fungal isolate (P. kudriavzevii zibd3) as the pathogen's capacity to infect and grow within the host is directly impacted by the temperature (Thomas & Jenkins 1997). Egg, larvae, pupae and adults of Z. indianus can be maintained at a wide range of temperatures enabling us to determine the effect of temperature on the host-pathogen interactions.

A broad range of temperatures were tested against the developmental duration of Z. indianus which showed significant variation in total developmental days (egg to adult) from average of 29.77 days at lowest temperature (17◦C) to lowest duration (11 days) at highest temperature (31◦C). Overall, temperatures around 25°C-28◦C are the thermal optimum for Z. indianus egg-to-adult development, allowing for faster development and high viability which is consistent with the findings of Silveira Neto et al. (1976), who demonstrated the optimal temperatures for insect development in tropical conditions within the range of 22◦C and 28◦C. Our findings were consistent with the earlier studies where the developmental period and viability of Z. indianus varied depending on the temperature range from 18◦C, 20◦C, 22◦C, 25◦C, 28◦C, 30◦C to 32◦C. The study found that with an increase in temperature from 18◦C to 30◦C, embryonic duration was shortened from 1.23 days to 0.49 days, while there was no change at 32°C, demonstrating temperatures greater than 30°C lethal for the egg stage, while lower threshold temperature for egg, larval and pupal development is 9.5◦C. Perhaps, the Z. indianus life stages were much less viable at temperatures above 32°C than they are at lower temperatures (Nava et al. 2007). Hence, the life cycle of Z. indianus, as in case of other ectotherms, differs in duration, viability and reproduction potential depending upon the temperature. The fungal species, P. kudriavzevii isolate zibd3, isolated from local population of Z. indianus from Chandigarh (T_avg= 31◦C) with maximum fungal association frequency, showed an inverse but rapid growth pattern at all tested temperatures taking minimum of 5 days at extreme lowest temperature and an average of 1.5 days at 31◦C. This may be due to the low association frequency of P. kudriavzevii found with local population of Z. indianus from other geographical locations of Solan and Shimla having T_avg equal to 21.3◦C and 17.6◦C, respectively, as the optimum growth temperature for P. kudriavzevii ranges from 30◦C-45◦C. Though, microbial pathogens have the ability to thrive under a broad spectrum of temperature, radiation and pH inhabiting diverse range of hosts (Yamagishi et al. 2018), studies also supports the thermo-tolerant property of various strains of P. kudriavzevii as it can bear thermal stress as high as 45°C (Chamnipa et al. 2018; Choi et al. 2017; Pongcharoen 2022). The literature provides evidence of the association of various species of Pichia with the larvae of Queensland fruit fly (Q fly), Bactrocera tryoni (Majumder et al. 2020), Drosophila suzukii (Hamby et al. 2012) and from eggs of Mexican Fruit Fly, Anastrepha ludens (Salas et al. 2018) with a relative abundance of around 43% (most abundant and ubiquitous), but the temperature-dependent studies of P. kudriavzevii with fruit fly species are scarce.

The overall increase in temperature has led to ecological shifting of geographical boundaries of insect population. Besides the abiotic stresses like temperature, native population also face biotic stresses such as microbial infections which induces various physiological and behavioural responses within the insect population. Temperature could impact fungi infection by decreasing and increasing fungi growth (Linder et al. 2008). Low temperature (17◦C) reduced the infectivity and growth kinetics of the fungi (slow growth) as compared to higher temperature (31◦C). Reproductive success of Z. indianus was significantly reduced in the presence of the fungal infection at high temperatures. This is probably due to the fact that colder temperature can benefit insect towards stronger immune response against microbial pathogens more than supressing the microbial growth as reviewed by Linder et al. (2008). Our data suggests that the interaction of fungal infection and temperature posed a substantial effect on the life history traits of Z. indianus, though the effect of fungal treatment alone was more prominent as compared to the temperature effect. Egg hatchability and viability were the most affected traits which directly influenced the adult emergence rate, while fecundity was not much affected when exposed to the fungal treatment alone. The data suggests that similar to the temperature effect on developmental stages of Z. indianus, the embryonic stages are most affected by the fungal infection though synergistic effect of temperature and fungal infection played a significant role in reducing fitness of Z. indianus, which might explain the plausibility of its biological invasion from tropical to temperate regions. Earlier studies also support the temperature-dependent physiological modifications in Z. indianus (Gupta) where a temperature increase of just 0.6◦C showed a significant increase in population viability and decrease in developmental duration (Ramniwas et al. 2012), while it significantly affects the reproductive potential of Z. indianus. At extreme constant temperatures (28–31◦C), Z. indianus males became sterile leading to the production of non-viable sperms though recovered fertility when males acclimatized to a normal temperature (25◦C). There are limited studies where combined effect of temperature and fungal infections are being studied with Z. indianus, however, it has already been reported with D. melanogaster (Linder et al. 2008) where, flies when subjected to cold treatment survived longer to infection by entomopathogenic fungus (EPF), Beauveria bassiana (Le Bourg et al. 2009), while flies seek out cooler temperatures when infected with Metarhizium robertsii possibly due the fact that the colder temperatures were detrimental to the pathogen as compared to the control flies which preferred warmer temperatures (Hunt et al. 2016). The pre-adult stages of various moth species such as Christoneura rosaceana (Isman and Fitzpatrick, 1995) and Thaumetopoea wilkinsoni (Yilmaz et al. 2013), survive better to Bacillus thuringiensis infections when maintained under cooler compared to warmer temperature. However, effects of temperature and fungal infection on life history traits are limited in case of fruit fly species but already been explored in case of other insect pests such as earwig larvae (Forficula auricularia) (Coulm and Meunier 2021) and granivorous cowpea weevil (Callosobruchus maculatus F.) in stored chickpea (Zahra et al. 2023), where temperature considerably affected the population of arthropod pests but higher temperatures favoured more fungi developments. Hence, our study is in corroboration with the earlier studies and is the first demonstration of dual stress of fungal and temperature under which Z. indianus could thrive where both the factors interact to alter the survival and reproductive potential of the fly and gives the possible explanation of invasion of this secondary pest in new ecological niches.

In the present study, effect of dual stressors (biotic and abiotic), temperature and fungal infection was demonstrated which had profound impact on developmental success of Z. indianus leading to an adaptive response. Overall, the findings show that the fungal infection has significant consequences on adult emergence, fecundity and egg hatchability of Z. indianus leading to a complex interaction of host-pathogen in ecology. These results may contribute to implement control measures aimed at controlling pest species of Drosophila, Z. indianus using fungal pathogens which can thrive better at broad range of temperatures. Further research is recommended to determine the molecular mechanism behind the reduced life cycle attributes caused by abiotic and biotic stress in infected flies. Understanding the physiological and behavioural mechanisms by which organisms react to biotic and abiotic stresses is precisely explained by the information presented here. In conclusion, the findings open up the avenues of fundamental and applied implications to the management of pest species of Drosophila by exploring the host-pathogen interaction under laboratory conditions.

1. Ethics approval and consent to participate

Not applicable.

2. Consent for publication

Not applicable.

3. Availability of data and materials

All data generated or analysed during this study are included in this published article.

4. Competing interests

There are no competing financial interests or personal relationships that could have influenced the work reported in this paper.

5. Funding

Not applicable.

6. Author Contributions

All authors read and approved the final manuscript.

7. Acknowledgments

This work was supported by Chandigarh University, Gharuan, Punjab, India.

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Effects of Pichia kudriavzevii on development, larval mortality and adult fecundity of Zaprionus indianus (Diptera: Drosophilidae) at different temperatures.

Status:

Journal Publication

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Abstract

Figures

1. INTRODUCTION

2. METHODS

2.1. Insect Collection and Rearing

2.2. Isolation and Identification of Fungi

2.3. Preparation of Fungal suspension

2.4. Fungal Growth rate at different temperatures

2.5. Impact of temperature on development time of Z. indianus

2.6. Impact of temperature and fungi on the life history traits of Z. indianus

2.7. Impact of temperature and fungi on the Fecundity of Z. indianus

2.8. Statistical analysis

3. RESULTS

3.1. Isolation and identification of fungi

3.2. Impact of temperature on development of fungus

3.3. Impact of temperature on development of Z. indianus

3.4. Impact of temperature and fungus on life history traits of Z. indianus

3.4.1. Total development period of Z. indianus

3.4.2. Egg hatchability and viability

3.4.3. Adult emergence of Z. indianus

3.4.4. Fecundity of Z. indianus

4. DISCUSSION

5. CONCLUSION

Declarations

References

Status:

Journal Publication

Version 1