Abstract
While biotic conditions are recognised contributors to the growth and production of the black soldier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae), abiotic conditions are arguably of equal or greater relevance. Shifts in key environmental conditions can be the difference between optimal production of a black soldier colony, or its collapse. As with all insects, the impact of these criteria is highly dependent on development stage of the insect and scale of application (e.g. growth chamber in a laboratory versus an industrial rearing room). Through the analysis presented herein, the impact of three abiotic factors (temperature, humidity, and photophase) on immature black soldier flies will be discussed as a means to serve as a model for investigating other abiotic factors contributing to the physiology of the species. By identifying the impact of these factors on black soldier fly development, the industry can optimise production, minimise financial investment, and enhance the economic and environmental returns of the system.
1 Introduction
Over the past seven decades, numerous studies have been conducted on the black soldier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae), resulting in a changing perspective of the insect: from a pest to beneficial (Tomberlin and van Huis, 2020). The combined impact of these studies has culminated in the proclamation that this species is the ‘crown jewel’ of the insects as food and feed industry (Tomberlin and van Huis, 2020), due to the fact that larvae of the species are able to upcycle numerous waste streams into a vast array of valuable products (Makkar et al., 2014; Surendra et al., 2016), while reducing the negative impact of these organic residues on air (Beskin et al., 2018; Perednia et al., 2017), land, and water quality (Elhag et al., 2022). Furthermore, given the flexibility of the system, the use of this insect to recycle organic waste streams and produce products of value can be applied by anyone globally, regardless of socioeconomic settings (Sheppard et al., 1994) if the environmental conditions under which the insects are reared are suitable.
The impact of rearing temperature on time to eclosion (d) for black soldier fly eggs. * Chia et al. (2018) and Sheppard et al. (2002) reported a similar time to eclosion (3.5 d) at 30 °C, which is why no marker is visible for Sheppard et al. (2002).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impacts of temperature, humidity, and photoperiod on the growth and development of immature black soldier flies will be discussed, as these three abiotic factors are likely the most important regulating development of the species. These three parameters are also those most commonly controlled or manipulated in the rearing of insects, at both laboratory and industrial scales. However, even though thousands of papers have been published on the black soldier fly, relatively few have specifically investigated these three parameters of interest.
2 Environmental conditions impacting development
Temperature
Temperature likely represents the most well-studied environmental parameter regulating insect development. It is well documented that there is generally an inverse relationship between insect development and temperature: at lower temperatures the development rate is reduced, and at higher temperatures, increased (Blanckenhorn et al., 2021; Couret et al., 2014; Sharpe and DeMichele, 1977; Wagner et al., 1984). However, this relationship is not always so, as there are certainly lower and upper thermal limits of development: points that can result in stasis, knockdown, injury, or even death of the insect (Angilletta, 2009). The impacts of a given temperature also vary depending on the stage of development of the insect.
The impact of temperature on development of black solder fly eggs has been studied or noted across a range of temperatures, from 10-42 °C. Within this range, the duration of development is inversely related to rearing temperature, and successful development of eggs has not been found below 15 or above 40 °C (Figure 1). Only two studies referenced in Figure 1 (Chia et al., 2018; Holmes et al., 2016) present data on the impact of temperature on egg survivorship (Figure 2). At temperatures between 19 and 35 °C, the eclosion rate is ∼60% or greater, and ∼10% or less at temperatures outside of this range. Within this temperature range of peak eclosion (19-35 °C), the mean duration of egg development is 4.51 ± 0.63 d.
The impact of rearing temperature on survival of black soldier fly eggs.
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of exposure to 4 °C on survival (mean ± standard error) of black soldier fly eggs. Adapted from Villazana and Alyokhin (2019).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of exposure to −12°C on survival (mean ± standard error) of black soldier fly eggs. Adapted from Villazana and Alyokhin (2019).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of cooling black soldier fly eggs for 24 hours on survivorship (mean ± standard error), over the course of embryonic development. Modified from Tollenaar et al. (2022).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of rearing temperature on larval development of the black soldier fly, when reared on grain-based diets. Note: development times at temperatures below 15 °C are not presented, as eggs held at those temperatures did not hatch, so no larvae were available to be reared at those temperatures.
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
Villazana and Alyokhin (2019) investigated the impact of short-term exposure to low temperatures on egg survival and found that eggs were quite susceptible to cold temperatures (Figures 3 and 4). Exposure to 4 °C for 24 h resulted in almost a 75% reduction in survivorship in comparison to the control (26 °C), while exposure for greater than 48 h resulted in less than 2% survival overall (95% reduction in comparison to the control) (Figure 3). Exposure to −12 °C had even greater impacts on egg survival (Figure 4). Exposure for a period as short as 10 min decreased survival by ∼80% in comparison to the control (less than 4% survival overall).
Tollenaar et al. (2022) tested the impact of cold storage on black soldier fly eggs, with an emphasis on the industrial application of such a process (Figure 5). They determined that storage of eggs at 10 °C and 80% relative humidity delayed eclosion by one day (in comparison to the control eggs, kept at 30 °C and 80% relative humidity), which would allow for more flexibility in the work week for an industrial producer, where egg eclosion must be synchronised with food source availability (i.e. organic waste streams) to prevent the waste of either. Tollenaar et al. (2022) also determined that egg survival was greater than 70% if chilling occurred 38 h after oviposition (after the eyespots have become visible), and when chilling began at 45-51 h after oviposition (after the mouth hooks have become visible), egg survivorship was greater than 80%.
The impact of temperature on larval development has also been well documented across the same temperature range as egg development (between 10 and 42 °C) (Figure 6). At temperatures below 34 °C, there is a general inverse relationship between temperature and development time. It can often be difficult to make comparisons across studies, as the rate of development is an interactive effect between rearing temperature and food source, and the diet used to raise the larvae can be quite variable. Additionally, the temperature of the food source/rearing substrate can deviate from the rearing (ambient) temperature, further impacting the development rate of the insects (Bosch et al., 2020; Gold et al., 2020; Yakti et al., 2022), but these crucial temperature data are rarely reported. However, numerous studies have been conducted on grain-based diets (i.e. Gainesville diet (Hogsette, 1992), spent brewer’s grains, chicken feed) at temperatures between 24 and 30 °C (Figure 7), but further variation in experiment design such as rearing container choice, larval density (Yakti et al., 2022), and sampling protocols can all impact the environmental conditions, and subsequent data that are generated.
The impact of rearing temperature on larval development of the black soldier fly, when reared on grain-based diets, at temperatures between 24 and 30 °C. Circular markers represent studies where larvae were fed Gainesville diet, square markers represent studies where larvae were fed spent brewer’s grains, and triangular markers represent studies where larvae were fed chicken feed.
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
Researchers also use different landmarks in development to determine when to cease measuring larval growth and development, further complicating comparisons that can be drawn across studies (Bosch et al., 2020). Some studies do not identify or quantify a marker/time point (Chia et al., 2018; Diener et al., 2009; Holmes et al., 2013), while others record larval development as time to first observation of prepupae (Nguyen et al., 2013; Oonincx et al., 2015), time to 25% of the population to reach the prepupal stage (Harnden and Tomberlin, 2016), or time to 40% of the population to reach the prepupal stage (Cammack and Tomberlin, 2017; Tomberlin et al., 2009). Even when experiments are conducted as similarly as possible, variation exists that cannot be explained by rearing temperature, diet, or sampling protocol, as seen in Figure 7 at 28 and 30 °C.
Villazana and Alyokhin (2019) also investigated the impact of short-term exposure to low temperatures on larval survival and found that larvae were much more tolerant to cold temperatures than were eggs (Figures 8 and 9) (larval treatments consisted of 100 larvae, placed in a 10 × 12.7 × 5 cm plastic tray containing 50 ml of vermiculite; egg treatments consisted of a 120 ml plastic cup containing a wet paper towel, on top of which was placed a piece of wax paper holding ∼1,000 eggs). When exposed to 4 °C for up to 48 h, larval survival was 89% or greater for all three stadia tested. Only after 72 h of exposure did survivorship drop significantly; only 2% of second instars survived, but 81 and 91% of third and fifth instars, respectively, survived after 72 h at 4 °C (Figure 8). When exposed to −12 °C for 10 min, larval survival was greater than 91% (Figure 9). However, survival dropped significantly when exposed for 30 or 60 min. Although larvae did survive exposure for 30 min, the impacts were quite variable, with no clear reason as to why. For some species, smaller individuals have lower supercooling points, making them less susceptible to cold temperatures; additionally, the supercooling point can be impacted by prior cold exposure, and seasonality (Johnston and Lee Jr, 1990). However, this aspect has not yet been tested or demonstrated in black soldier flies, and the relationship does not appear to be linear, at least for different exposure durations at −12 °C or across all larval stadia, where second instars had much greater survival than first or fifth instars.
The impact of exposure to 4 °C on survival (mean ± standard error) of black soldier fly larvae. Adapted from Villazana and Alyokhin (2019).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of exposure to −12 °C on survival (mean ± standard error) of black soldier fly larvae. Adapted from Villazana and Alyokhin (2019).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of relative humidity on time to eclosion (d) for black soldier fly eggs when reared at approximately 27 °C. Adapted from Holmes et al. (2012).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of relative humidity on survival of black soldier fly eggs (mean ± standard error) when reared at approximately 27 °C. Adapted from Holmes et al. (2012).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
Humidity
The impact of humidity on the life-history of black soldier flies is largely unstudied; only one previous study has specifically investigated this topic: Holmes et al. (2012). At ∼27 °C (incubator setpoint, actual mean temperatures ranged from 27.36-28.19 °C), egg development rate and survivorship were positively correlated with an increase in relative humidity (Figures 10 and 11, respectively). Data presented by Harnden and Tomberlin (2016) align well with the development data presented by Holmes et al. (2012), as they reported 100 h to eclosion when eggs were kept at 27.6 °C and 55% relative humidity. At 25 °C and 70% relative humidity, Chia et al. (2018) reported approximately 60% survival of eggs, which also falls within the range presented by Holmes et al. (2012).
No studies have investigated the impact of relative humidity on larval development, likely because the moisture content of the larval food source is a more important factor. However, the relative humidity of the rearing environment will directly impact the moisture content of the diet: as relative humidity decreases, evaporation of the moisture in the diet increases. No clear patterns are visible yet within the literature, even when comparing studies conducted on the same source population and diet (Figure 12). Additional factors such as ambient temperature, airflow, SA:V of the food source can also influence the rate at which the moisture content of the larval food source will change.
The impact of relative humidity on development of black soldier fly larvae when fed Gainesville diet at different temperatures.
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
For the postfeeding stages of immature development, stage duration is negatively correlated with relative humidity (Holmes et al., 2012) (Figure 13). The duration of the prepupal stage is approximately 10% shorter at 70% than 25% relative humidity, while the impact on the pupal stage is much less pronounced (∼6% faster development at 70% humidity). Humidity has much greater impacts on survival (Figure 14). Mortality of prepupae and pupae was 62% and 65%, respectively, when reared at 25% relative humidity, in comparison to 3 and 2%, respectively, when reared at 70% relative humidity.
The impact of relative humidity on development (mean ± standard error) of black soldier fly prepupae and pupae. Modified from Holmes et al. (2012).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of relative humidity on survival (mean ± standard error) of black soldier fly prepupae and pupae. Modified from Holmes et al. (2012).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
Photophase
While most research on black solder flies and light has been conducted with regard to adult mating success (Meneguz et al., 2023), only one study has specifically investigated the impacts of photoperiod on the life history of black soldier flies: Holmes et al. (2017). They found that increased light exposure results in decreased development time for all immature life stages (Figure 15). However, it should be noted, that despite using temperature regulated growth chambers for the experiments (set at 27 °C), mean temperatures differed significantly between light exposure treatments over the course of the experiment (0 h: 26.35 °C, 8 h: 27.23 °C, 12 h: 28.34 °C). When reared in complete darkness, adult emergence was significantly lower (72%) in comparison to the other two treatments (>95% emergence). The studies mentioned previously in this review generally utilised either 12 or 14 h of light exposure during their experiments (Figure 16), likely minimizing the impact of reduced photophase duration on the post feeding stages. Unfortunately, plotting the data in Figure 1 based on photophase duration (Figure 16) does not provide insight into the differences in larval development seen across these studies when conducted at the same temperature. The expected trend (faster development with increased photoperiod) occurs at 28 °C, but not at 30 °C.
Mean development time (days) ± standard error for the different immature life stages of the black soldier fly, in response to photophase duration. Modified from Holmes et al. (2017).
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
The impact of photoperiod on development of larval black soldier flies, across a range of temperatures. This figure can be cross referenced with Figure 6 to identify the study/citation corresponding to each data point.
Citation: Journal of Insects as Food and Feed 10, 10 (2024) ; 10.1163/23524588-20230026
3 Conclusions and recommendations
As with any insect, development is impacted by a host of abiotic conditions. As discussed, a key factor that has historically received the most attention with the black soldier fly but can serve as a model for exploring other factors, is temperature (Chia et al., 2018; Tomberlin et al., 2009). However, the degree of impact, while being stage specific (e.g. egg vs adult, larvae vs pupae) (Holmes et al., 2010), is also governed by age within stage, size, and sex (Addeo et al., 2022; Angilletta, 2009; Blanckenhorn et al., 2021). Unfortunately, broad generalizations as to what temperature is needed to optimise larval development is truly challenging. For example, 7 of the 10 studies referenced in Figure 6 utilised insects from the same originating population, and variation is still present between these studies. Although Kaya et al. (2021) revealed that most captive populations of black soldier flies worldwide are descended from this same population, the variation seen across something as simple as ‘the impact of temperature on larval development’ indicates that caution must be used when comparing and applying data from published studies to that being found in any rearing environment (laboratory or industrial). These published studies are undoubtedly useful, and provide valuable information, but data from previous research should be validated on any captive population, regardless of origin.
Populations of other fly species, even across a small geographic range spanning ∼300 miles (2.6 degrees latitude and 3.2 degrees longitude), have been shown to be quite unique in terms of their responses to temperature (Owings et al., 2014). Additionally, responses to photophase duration differ even across genera within the same family for species (Bauer et al., 2020; Nabity et al., 2007) that fill the same ecological niche as black soldier flies; such differences are probably common across many populations and species. With that said, responses of black soldier flies to other abiotic factors including, but not limited to, diet pH (Meneguz et al., 2018), airflow, temperature fluctuations (i.e. mimicking a natural diel cycle), chemical compound production and exposure (e.g. CO2 and NH3) likely influence development and still require additional investigation. In the end, by deciphering the impact of these abiotic factors on black soldier fly development, efforts can be made to coordinate these conditions collectively as a means to optimise production, while minimizing the associated expenses of black soldier fly production. However, considerable effort is still needed to determine how these conditions covary across life stage, sex, population, and scale.
In order to best move our industry forward, we make the following recommendations to strengthen future research on the three abiotic parameters discussed.
Temperature
- ∙ Conduct studies using uniform distributions. For example, Chia et al. (2018) generally conducted experiments with temperatures that were 5 °C apart, but some intermediate levels were used (2-3 °C difference from lower and higher temperatures tested), while the range of temperatures tested by Holmes et al. (2016) were 3 or 4 °C apart, and Tomberlin et al. (2009) studied development at temperatures 3 or 6 °C apart.
- ∙ Conduct more refined development studies within the range of 24-32 °C; we suggest at temperature intervals of 2 °C.
- ∙ Collect temperature data of the rearing substrate/larval food source during the course of experiments, as these temperatures are generally different from ambient, and likely have a more direct impact on the developing insects than the ambient temperature/rearing chamber setpoint.
- ∙ Conduct experiments that have industry relevance/impact and are based on stakeholder (i.e. industry) input. This will no doubt be enhanced by the recently formed Center for Environmental Sustainability through Insect Farming, whose main charge is to conduct research with direct industry input.
Humidity
- ∙ Conduct research on the impacts of relative humidity on larval development. We recognize that research in this area is complicated, given the number of additional biotic and abiotic factors that can (and do) interact to impact the humidity of a given rearing experiment or environment. However, given the lack of current knowledge on this topic, the possibilities here are endless, and the research is much needed.
Photophase
- ∙ Conduct research that reflects the natural history of the species. The summertime daylength within the native distribution of H. illucens ranges from 12-16 h. Refined research on photophase exposure within this range could greatly enhance the rearing of the species while at the same time potentially reduce the resources (i.e. electricity) needed for rearing, which would have an additional positive impact on the environment.
-
∙
Conduct refined research on the impact of light on black soldier fly development, such as:
- o Eliminating artifacts of increased temperature within light exposed treatments/experiments, to ensure the parameters of interest (i.e. photophase) are not being influenced by an interactive effect with other abiotic conditions.
- o Investigating the impact of wavelength, intensity, and other parameters on the immature stages, as has been done with the adult stage. Refinement in this area could also result in decreased energy usage.
Corresponding author; e-mail: jacammack@evoconsys.com
Acknowledgements
We would like to thank the Organisation for Economic Co-operation and Development for providing funding to JAC to present this work at the 2022 Insects to Feed the World Conference, Grant Vandenberg and Laura Gasco for organizing the conference symposium, and the other symposium speakers for valuable discussion before, during, and after the conference that is helping to advance our science and industry.
Conflict of interest
The authors have declared no conflict of interest.
OECD disclaimer
This paper was given at the workshop Development of standard research methodologies for the mass rearing of insects fed waste organic residues for the production of novel animal feeds, which took place in Quebec, Canada, on 12-16 June 2022, and which was sponsored by the OECD Co-operative Research Programme: Sustainable Agricultural and Food Systems whose financial support made it possible for the author to participate in the workshop.
The opinions expressed and arguments employed in this paper are the sole responsibility of the authors and do not necessarily reflect those of the OECD or of the governments of its Member countries.
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