Discussion
Our results indicate that biodegradable plastics are not any better than common plastics. This is based on the adverse outcomes to fitness after consuming either plastic oil-derived or compostable plastics for almost all fitness variables. More specifically: compared to the control group, consuming these products delayed the developmental duration of both larval and pupal stages, hastened animal mortality, which resulted in lower weight (with the lightest in the PS and CP groups), and led to reduced survival. We will discuss each of these different effects below.
One negative effect of consuming plastics oil-derived and bioplastics is the delay in developmental time. Although, the presence of micro- and oil-derived nanoplastics did not influence larval growth in Bombix mori (Muhammad et al., 2021). A similar result was reported in T. molitor and Hermetia illucens larvae after eating bioplastics (Heussler, et al. 2024; Kokalj et al. 2024). Our results showed that both types of plastics delay the development time. The differences could be explained by time, since our animals fed on both types of plastic from very early larval stages compared to previous studies. One related question is that of the cost of delayed development. A consequence is that animals can face more threats, such as predators, parasites, and/or parasitoids (Nylin and Gotthard, 1998). Increasing development times is common in insects, largely explained by not reaching a certain body mass threshold necessary to complete metamorphosis (Nijhout, 2003). This aligns with our result of reduced weight in animals that consumed plastics or compostable products: reduced weight could prolong development. There are several non-mutually exclusive mechanistic explanations for this. First, stressed animals may not gather enough or do not have access to particular nutrients for their development (e.g. Welden and Cowie, 2016). Second, the presence of toxic elements in both petroleum-derived and compostable plastics may cause negative effects (Wang et al., 2020; 2021; Zimmermann et al., 2021). Third, either plastics or compostable products may obstruct the digestive system and impede nutrient acquisition (Sigler, 2014). And fourth, plastics may affect the animal’s microbiota (Antonelli et al., 2022).
Our results also showed that mortality increased when larvae were fed with biodegradable and non-biodegradable plastics, where even mortality was higher in the CP group. Similar studies showed that Drosophila melanogaster males had a higher mortality compared to females after ingesting PS microplastics (El Kholy and Al Nagar, 2023). In contrast, in yellow mealworm beetles and black soldier fly larvae that were fed bioplastics did not show increased mortality (Heussler, et al. 2024; Kokalj et al. 2024). However, similar to other studies (Wang et al., 2021), we found a trade-off between investment in development and survival. Also, the number of offspring after reproduction in surviving pairs of treatment groups was significantly lower than control. As explained above, the trade-offs may be understood by the different mechanisms underlying the ingestion of non-natural material. One challenge to clarify is how the different effects plastics non-biodegradable and bioplastics can cause on survival, reproduction, and growth may balance each other, resulting in some traits being less affected than others. For example, we are aware of the effects of oil derived microplastics on antioxidative stress response, sex hormone disruption, and disturbed transcription of steroidogenic genes as main drivers of impaired reproduction (Wang et al., 2021). How these effects may be balanced with the effects of the same material on, say, survival, is unclear. One other challenge is to explain whether the observed trade-offs are adaptive or are an artifact of an animal being unable, in general, to deal with, say, a toxic material.
Finally, the idea that plastic ingestion has detrimental effects on life history traits and that this can lead to apparent trade-offs is not new (Santos et al., 2021). What is new about our work is the trade-off and outcome of ingesting compostable, which plays as much a detrimental role as ingesting plastics. For example, animals may trade off fecundity for development time after eating compostable products. Why would compostable products produce similarly acute patterns as plastics? At the proximate level, compostable products may contain similarly toxic components to those of common plastics. It is known that added components to plastics produce inflammatory responses, endocrine disruption, neurotoxicity, oxidative stress, and metabolic alterations that all together affect immunity, reproduction, and digestion in insects (reviewed by Sánchez-Hernández, 2021). This may be the case for compostable products too. For example, a study analyzed 43 biobased and biodegradable products and found that 67% showed baseline toxicity, 42% led to oxidative stress, and 23% induced antiandrogenicity (Zimmermann et al., 2021).
Conclusions
Considering the assertion that compostable products can serve as an alternative to conventional plastics, our work presents contradicting evidence: insects fed with compostable products may experience fitness effects (growth, fecundity, and survival) as detrimental as those observed in insects fed with plastics. The cause of this phenomenon is currently unknown, and one potential explanation is the presence of added toxic components in compostable products. Consequently, our work serves as a cautionary note against the argument advocating for the safety of using compostable materials.
Acknowledgements
This project was financed by a UNAM-PAPIIT grant IN204921.
References
Antonelli, P., Duval, P., Luis, P., Minard, G., & Valiente Moro, C. (2022). Reciprocal interactions between anthropogenic stressors and insect microbiota. Environmental Science and Pollution Research, 29 (43), 64469-64488 https://doi.org/10.1007/s11356-022-21857-9
Andrady, A.L. and Neal, M.A., 2009. Applications and societal benefits of plastics. Phil. Trans. R. Soc. B, 36: 1977-1984 http://doi.org/10.1098/rstb.2008.0304.
Arikan, E.B. and Ozsoy, H.D., 2015. A review: investigation of bioplastics. Journal of Civil Engineering and Architecture 9: 188-192 http://doi.org/10.17265/1934-7359/2015.02.007.
Atiwesh, G., Mikhael, A., Parrish, C.C., Banoub, J. and Le, T.A.T., 2021. Environmental impact of bioplastic use: A review. Heliyon, 7, e07918 https://doi.org/10.1016/j.heliyon.2021.e07918.
Castro-León, I., Cervantes-Mayagoitia, J.F., Schettino-Bermúdez, B.S. and Nogueda-Hernández, N., 2017. Comparación de cinco dietas alimenticias en la cría de Tenebrio molitor L. (Coleoptera: Tenebrionidae). Entomología Mexicana, 4, 616-620 https://acaentmex.org/entomologia/revista/2017/EV/EM0772017_616-620.pdf.
El Kholy, S. and Al Naggar, Y., 2023. Exposure to polystyrene microplastic beads causes sex-specific toxic effects in the model insectDrosophila melanogaster . Scientific Reports, 13, 204 https://doi.org/10.1038/s41598-022-25057-w.
Frooninckx, L., Berrens, S., Van Peer, M., Wuyts, A., Broeckx, L. and Van Miert, S., 2022. Determining the effect of different reproduction factors on the field and hatching of Tenebrio molitor egg. Insects, 13, 615 https://doi.org/10.3390/insects13070615.
Gotelli, N.J., 1995. A primer of ecology. Sunderland, Massachusetts: Sinauer Associates Incorporated, pp.xvi, 206.
Han, X., Zheng, Y., Dai, C., Duan, H., Gao, M., Ali, M.R. and Sui, L., 2021. Effect of polystyrene microplastics and temperature on growth, intestinal histology and immune responses of brine shrimp Artemia franciscana . Journal of Oceanology and Limnology, 39, 979-988 https://doi.org/10.1007/s00343-021-0357-8.
Martinho, S.D., Fernandes, V.C., Figueiredo, S.A. and Delerue-Matos, C., 2022. Microplastic pollution focused on sources, distribution, contaminant interactions, analytical methods, and wastewater removal strategies: A review. International Journal of Environmental Research and Public Health, 19, 5610 https://doi.org/10.3390/ijerph19095610.
Matyja, K., Rybak, J., Hanus-Lorenz, B., Wróbel, M. and Rutkowski, R., 2020. Effects of polystyrene diet on Tenebrio molitor larval growth, development and survival: Dynamic Energy Budget (DEB) model analysis. Environmental Pollution, 264, 114740 https://doi.org/10.1016/j.envpol.2020.114740.
McConnel, G., Lawson, J., Cañas-Carrell, J.E. and Brelsfoard, C.L., 2023. The effects of nano and microplastic ingestion on the survivorship and reproduction of Aedes aegypti (L.) and Aedes albopictus (Skuse). bioRxiv, 2023-06 https://doi.org/10.1101/2023.06.23.546347.
MacLeod, M., Arp, H.P.H., Tekman, M.B. and Jahnke, A., 2021. The global threat from plastic pollution. Science, 373, 61-65 https://www.science.org/doi/full/10.1126/science.abg5433.
Muhammad, A., Zhou, X., He, J., Zhang, N., Shen, X., Sun, C., … and Shao, Y., 2021. Toxic effects of acute exposure to polystyrene microplastics and nanoplastics on the model insect, silkwormBombyx mori . Environmental Pollution, 285, 117255 https://doi.org/10.1016/j.envpol.2021.117255.
Nylin, S. and Gotthard, K., 1998. Plasticity in life-history traits. Annual Review of Entomology, 43: 63-83 https://doi.org/10.1146/annurev.ento.43.1.63.
Nijhout, H.F., 2003. The control of body size in insects. Developmental Biology, 261, 1-9 https://doi.org/10.1016/S0012-1606(03)00276-8.
Pölkki, M., Krams, I., Kangassalo, K. and Rantala, M.J., 2012. Inbreeding affects sexual signalling in males but not females ofTenebrio molitor . Biology Letters, 8, 423-425 https://doi.org/10.1098/rsbl.2011.1135.
Sanchez-Hernandez, J.C., 2021. A toxicological perspective of plastic biodegradation by insect larvae. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 248, 109117 https://doi.org/10.1016/j.cbpc.2021.109117.
Santos, R.G., Machovsky-Capuska, G.E. and Andrades, R., 2021. Plastic ingestion as an evolutionary trap: Toward a holistic understanding. Science, 373, 56-60 https://doi.org/10.1126/science.abd7012.
Stearns, S.C., 1989. Trade-offs in life-history evolution. Functional Ecology, 3, 259-268 https://doi.org/10.2307/2389364.
Sun, Y., Qian, Y., Geng, S., Wang, P., Zhang, L. and Yang, Z., 2023. Joint effects of microplastics and ZnO nanoparticles on the life history parameters of rotifers and the ability of rotifers to eliminate harmful phaeocystis. Chemosphere, 310, 136939 https://doi.org/10.1016/j.chemosphere.2022.136939.
Sigler, M. (2014). The effects of plastic pollution on aquatic wildlife: current situations and future solutions. Water, Air, & Soil Pollution, 225, 1-9 https://doi.org/10.1007/s11270-014-2184-6
Varg, J.E., Kunce, W., Outomuro, D., Svanbäck, R. and Johansson, F., 2021. Single and combined effects of microplastics, pyrethroid and food resources on the life-history traits and microbiome of Chironomus riparius . Environmental Pollution, 289, 117848 https://doi.org/10.1016/j.envpol.2021.117848.
Wang, Z., Dong, H., Wang, Y., Ren, R., Qin, X., & Wang, S. (2020). Effects of microplastics and their adsorption of cadmium as vectors on the cladoceran Moina monogolica Daday: Implications for plastic-ingesting organisms. Journal of Hazardous Materials, 400, 123239. https://doi.org/10.1016/j.jhazmat.2020.123239
Wang, C., Zhao, J. and Xing, B., 2021. Environmental source, fate, and toxicity of microplastics. Journal of Hazardous Materials, 407, 124357 https://doi.org/10.1016/j.jhazmat.2020.124357
Wang, J., Zheng, M., Lu, L., Li, X., Zhang, Z. and Ru, S., 2021. Adaptation of life-history traits and trade-offs in marine medaka (Oryzias melastigma ) after whole life-cycle exposure to polystyrene microplastics. Journal of Hazardous Materials, 414, 125537 https://doi.org/10.1016/j.jhazmat.2021.125537
Welden, N. A., & Cowie, P. R. (2016). Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus . Environmental pollution, 218, 895-900. https://doi.org/10.1016/j.envpol.2016.08.020
Yang, Y., Yang, J., Wu, W., Zhao, J., Song, Y., Gao, L., Yang, R. and Jiang, L., 2015. Biodegradation and Mineralization of Polystyrene by Plastic-Eating Mealworms: Part 1. Chemical and Physical Characterization and Isotopic Tests. Environmental Science & Technology, 49,12080-12086. https://doi.org/10.1021/acs.est.5b02661
Zimmermann, L., Dombrowski, A., Völker, C. and Wagner, M., 2020. Are bioplastics and plant-based materials safer than conventional plastics? In vitro toxicity and chemical composition. Environment International, 145, 106066 https://doi.org/10.1016/j.envint.2020.106066
Tables
Table 1. Survival estimations obtained from the Multistate model with developmental stage as state and treatment as covariate.