The “Plastic Age”: From Endocrine Disruptors to Microplastics – An Emerging Threat to Pollinators

Abstract

Currently, human beings live in a new era, known as the “Plastic Age.” Throughout the history of plastics, two significant potential hazards to human health have been identified. Firstly, the endocrine-disrupting capability of monomers used in plastic synthesis has been under scrutiny. Secondly, in recent years, the potential dangers of nano- and microplastics released from the polymers themselves have begun to gain visibility, with their abundance and health consequences still under study. Consequently, this chapter begins with an analysis of xenobiotic compounds and endocrine disruptors. Subsequently, this chapter emphasizes the concept of microplastics, as their limited number of publications contrasts with their ubiquitous global distribution and potential harmful effects. Their presence across terrestrial ecosystems raises concerns about the possible impacts on pollinator health as these animals are crucial for maintaining agricultural production and plant biodiversity. The quantification of these particles in honey, beeswax, or the pollinators themselves could enable the assessment of the environmental impact of microplastics in terrestrial ecosystems, together with other pollutants that endanger these species. Nevertheless, more research is needed to evaluate the potential threat of microplastics and potential synergies among microplastics and other pollutants found in nature as a consequence of anthropogenic activities.

1. Introduction

Contemporary society exists in a distinct historical period, often referred to by some authors as the “Plastic Age”. This nomenclature stems from the ever-expanding influence of plastics, which are now imprinting a lasting mark on terrestrial and aquatic environments across the globe [1, 2]. In the present day, plastics have become a common feature in a wide range of everyday items, owing to the heavy dependence of various industries on plastic polymers. Plastics have become an integral part of our lives, influencing how products are packaged, transported, and utilized, while also driving technological advancements. The underlying issue is that their production, use, disposal, and recycling involve the release of various particles that have never been found in the natural environment or circulating in the population’s bloodstream until now. From a quantitative perspective, more than 200 compounds, called xenobiotic compounds, have been identified that should not be present within any living organism [3]. These compounds can be defined as:

“Organic chemicals that are not products of biosynthesis” [4] or

“A xenobiotic is a chemical which is not a natural component of the organism exposed to it. Synonyms: drug, foreign substance or compound, exogenous substance or compound” [5].

In light of their enduring presence and extensive distribution, an increasing number of authors are focusing their attention on the potential link between environmental xenobiotics and the development of various physiological disturbances or pathologies, with particular emphasis on exploring the deleterious effects of endocrine disruptors [6, 7, 8, 9, 10]. The concept of endocrine disruptors is relatively recent. While the knowledge of synthetic compounds capable of mimicking hormonal actions dates back to the early twentieth century, exemplified by bisphenol A (BPA),¹ it was not until the 1990s that the term was officially coined. It was during this period that a heightened awareness emerged regarding the potential association between exposure to environmental contaminants and an elevated risk of developing pathologies. The initial definition proposed by a public body, the United States Environmental Protection Agency² (EPA), characterizes an endocrine disruptor as:

“An exogenous chemical substance or mixture that alters the structure or function(s) of the endocrine system and causes adverse effects at the level of the organism, its progeny, populations, or subpopulations of organisms, based on scientific principles, data, weight-of-evidence, and the precautionary principle” [13].

Subsequently, successive definitions have been proposed by the European Union and the US Environmental Protection Agency [12, 14], or various institutions, such as the World Health Organization [15]. However, for The Endocrine Society,³ these definitions are problematic when placed in the context of hazard and risk characterization. Only one of them, the one made by the EPA (detailed in the previous paragraph), better fits the concept of endocrine disruptor as an external element influenced by environmental chemicals, capable of affecting the endocrine system in some way. Therefore, they propose a definition within the theoretical line of the EPA, but using simpler language:

“An ED is an exogenous chemical, or mixture of chemicals, that interferes with any aspect of hormone action” [12].

Currently, one of the most interesting and complete definitions of the concept can be found in Dr. Nicolás Olea’s book “Libérate de tóxicos” (Free yourself from toxics), which states:

“Endocrine disruptors are chemical substances capable of altering the synthesis, release, transport, metabolism, binding, action or elimination of natural hormones in the organism, i.e., with the ability to alter hormonal balance and the regulation of embryonic development and, therefore, with the potential to cause adverse effects on the health of an organism or its offspring.” (Translated from [16]).

Within the broad diversity of molecules that make up this new group of xenobiotics compounds, However, there is a changing trend in the study of plastics, since in recent years it has been observed that not only low molecular weight monomers can have an impact on human health, but that abrasive action on any plastic element could contribute to its disintegration, creating countless nano and micro scale particles [17].

2. Microplastics

The concept of “microplastics” (MPs) still lacks a universal definition, although it is common in the literature to define them as any plastic particles with a size smaller than 5 mm. When it comes to particles smaller than 1 μm in size, the term “nanoplastics” is often used [18, 19]. Hence, we can come across various nomenclatures used to define the same concept. Leslie et al. [18] employ the term “plastic particles” to avoid ambiguity, while Sripada et al. [20] use the term “nano- and microplastics (NMPs).”

These types of particles fall into the category of “contaminants of emerging concern” because they have been detected in the environment, may have an impact on ecosystems or human health, and are not yet regulated by environmental laws [21]. Microplastics have been identified in numerous settings, locations, and matrices. From the water, food, and air in our immediate surroundings to remote environments like mountains and seas, microplastics have become unwelcome guests in our lives [18, 21].

The most obvious consequence of the ubiquity of microplastics is human exposure, which is a clear reality as their presence has been detected in urine [22], feces [23], and even in human blood and placenta [18, 24].

However, the major issue concerning microplastics is the determination of the true extent of the problem, that is, the ability to realistically quantify microplastic pollution in the environment and, consequently, the potential danger that numerous animal and plant species, as well as humans, are facing.

3. Microplastics in terrestrial ecosystems

The first studies assessing the presence of MPs particles in natural environments have focused mainly in aquatic ecosystems and marine biota, which have received attention since these particles have been found in oceanic and coastal locations across the globe [25, 26, 27] as well as in freshwater [28]. Even though many studies have focused on the potential harm of MPs in aquatic ecosystems, studies on the effects of these particles in terrestrial ecosystems are increasing [29, 30]. Considering that most of the plastic waste originates on land as a result of anthropic activities [31, 32], it is logic to consider that MPs produce alterations and interact with species in these ecosystems as well. In fact, MPs can accumulate in soil, altering its biophysical environment [29, 33] and ultimately entering in the food chain.

Recent evidence is extremely concerning, as there are studies like Shan et al. [34], in which they have observed the ability of polystyrene nanoplastics to cross the blood-brain barrier and induce neurotoxicity in a mouse model study. Similarly, Jin et al. [35] administered polystyrene microplastics (PS-MPs) in drinking water to mice and observed the accumulation of these particles in the brains of the treated animals. Their findings suggested that PS-MPs could disrupt the blood-brain barrier, impair learning and memory, and induce neurotoxicity in mice. However, more research needs to be done on how results obtained from experiments translate to the concentrations found in nature [33].

Moreover, most studies have focused on how these compounds have an effect in humans and other mammals, while disregarding numerous wild species. In this sense, insects are the widest group of the animal kingdom and form the base of the trophic chain within terrestrial ecosystems. One of the services they provide to the environment, along with other species, is pollination. The omnipresence of MPs facilitates that pollinators contact these particles that adhere to their bodies while feeding on flowers on enter their bodies by drinking freshwater.

4. Importance of pollinators

Pollinators are key pieces of terrestrial ecosystems and underpin its successful functioning [36, 37]. A large number of plant species depend on these animals to fertilize and reproduce, and have co-evolved since ancient times [38], and these relationships are essential to maintain the ecological communities [39, 40]. Pollination can occur via wind or water, and via animal [38]. Although the abiotic factors are used by some species, it is estimated that nearly 90% of plants worldwide need animal pollination [41]. The communication between pollinators and plants is mutually beneficial, since pollinators feed on nectar and pollen, floral rewards, while enhance plant’s reproductive success by transporting pollen among flowers.

Pollination is crucial for agriculture, and in many countries, the use of insects is a common practice [42, 43]. Approximately, three quarters of agricultural production rely at least to some extent upon insect pollination [39, 44], and its worth is estimated in 235–577$ billion globally per year in crop and orchard pollination [44]. However, besides the economic value translated into food production, it is worth emphasizing the help in maintaining biodiversity.

On the one hand, honeybees (Apis spp.) and bumblebees (Bombus spp.) are the preferred and more widespread species used for pollination, although there are slight variations among continents [37]. Their adaptability and easy management make them very accessible to use. Moreover, in case of the honeybee, being a eusocial insect implies there might be thousands of individuals in a colony, which also facilitates their study, and it also provides hive products such as honey and wax, destined to human consumption. On the other hand, these two species are not the only ones found in the ecosystem. There are over 20,000 species of bees worldwide [43] and bees are not the only pollinators. Wild pollinators also comprise wild bees, flies, butterflies, beetles, wasps, moths and other insects as well as birds, bats and lizards. Wild pollinators have developed efficient pollinating systems and are of great importance since they pollinate crops more effectively [45].

5. Onset of research

The presence of NMPs in the terrestrial environment has become a huge concern for the scientific community and the general public. In these past years, the first studies have begun to analyze how the presence of these particles might influence pollinator health since one major outcome of the situation could be the disruption of plant-pollinator communication and the implications on biodiversity and food production. Many of the studies have been carried out in honeybees [46, 47, 48, 49] and it could be expected that similar effects occur in other insect pollinating species. MPs have been found in apiaries in China [49] and honeybees have been used as samplers for microplastics in Denmark in urban and suburban areas [50]. However, experiments on the effects of MPs are usually carried out under laboratory conditions with short-term exposure [51], and pollinators exhibit varying responses to different sizes and concentrations of NMPs [30, 52].

6. Problems with NMPs in pollinators

Problems with NMPs in pollinators have been mainly recorded in honey bees due to the benefits of studying this species, mentioned above. Moreover, research has been carried out primarily in the laboratory, where ingestion of MPs has shown to sometimes alter the size [49], the gut microbiota [46], and the susceptibility to viral infections [49].

Although behavioral changes have been observed in aquatic animals after MPs ingestion, studies carried out in honeybees are scarce and have shown somewhat discrepant results. Buteler et al. [53] did not detect behavioral changes after MPs ingestion whereas Balzani et al. [48] found changes in feeding behavior depending on the administered MPs-concentration.

Laboratory studies have found that exposure to MPs of 0.1 μm significantly decreased body weight of honeybees [54] and MPs particles of 0.5 and 5 μm induced hair fall and changes in body color of adult honeybees [49] as opposed to bigger particles. MPs accumulated in the digestive tract might produce intestinal dysplasia [54] and also enter to other body parts such as the Malphigian tubules and the trachea, possibly through breakdown of the peritrophic membrane of the midgut [49] and transported within the hemolypmph. This is of great concern since honeybee gut microbiota might interact with MPs accumulated in the distal part of the digestive tract, the hindgut [54], whereas breakdown of the peritrophic membrane might cause impairment of the intestinal barrier functions and accentuate susceptibility of viral infection. Gut microbiota in honeybees is important to maintain its health and it is involved in nutrition processes [55], growth [56], immunity [57] and protection against pathogens [58], as gut microbiota has been studied to have similar roles in other insects. Honeybees fed with MPs decreased alpha diversity of gut microbiota [46] and it could have negative effects on their physiology. At individual level under laboratory conditions, MP consumption seems to compromise the immunity response and to alter gene expression [46], suggesting a reduced capacity for detoxification of xenobiotics and other pathogens [49].

Besides the effects that MPs have on honeybees, it is important to note that particles are ubiquitous in nature and can be found in their bodies, attached in their cuticles or in the digestive tracts [50, 53] and in other matrices of the hive [47], dispersing them to all the colony. MPs are found in contaminated water and food, and it has been suggested that the gear of beekeepers is another contamination source. MPs are incorporated from the environment by adult workers when foraging and these particles can be found in larvae, probably through nursing and feeding the larvae. More research needs to be done in order to evaluate possible consequences. Another possibility that has been observed in mosquitoes is that larvae ingested MPs and these particles remained in their adult stage after metamorphosis [59]. Once ingested by the honeybees, MPs are incorporated to the hive and stored mainly in the wax, probably because of the hydrophobic properties of plastic [47]. MPs can also be found in honey. Alma et al. found no significant differences in the MPs concentration in honey from their experimental hives and commercial honey, suggesting there is no contamination from MPs stored in wax to honey. At the end of their experiment, they did not find differences in honey reserves and bee population between the treated and the untreated group neither. As particles are ubiquitous and honey bees shared floral resources with other pollinating insects, it would be expected that these species also had attached particles in their bodies that were carried and stored in their nests, posing similar threats.

Mortality in honeybees fed with MPs was not significantly higher than in control groups [46, 53] and might appear that MPs are not the most toxic pollutant. Nevertheless, sub lethal effects must be considered, since they might affect pollinator’s performance and fitness and have an impact on the immune response of honeybees. And it is a reason why mortality should be not used as an end point on colony performance. In this regard, López-Uribe et al. [60] proposed the term “pollinator health”. It was defined as “a state that allows individuals to live longer and/or reproduce more (…) thus providing more ecological services”, concept that uses other indicators and aspects of individual and colony performance of honeybees and other pollinators.

7. Other pollutants

MPs are able to adhere and to carry other xenobiotic compounds such as chemicals and pesticides, which increase the toxicity of MPs and mortality of pollinators [61]. Because of it, chemical effects could be greater than physical effects. For example, the use of the antibiotic tetracycline increased lethality in honeybees fed with MPs [46]. MPs are able to transport opportunistic bacteria that could harm the honeybee gut microbiota. In fact, the term “plastisphere” encompasses the microbial communities in plastic debris [62], and highlights the formation of ecosystems evolved to live in plastic environments. Besides bacteria and other microorganisms, MPs can adsorb other pollutants. Moreover, laboratory experiments tend to use spherical MPs particles whereas fibers have been also found in the field [49, 50]. Because fibers and other irregular shapes are more common in the environment, it is unclear how the concentrations, sizes and shapes used in experiments are representative in nature.

8. Considerations and future research perspectives

Honeybees have been traditionally used as a sentinel insect to monitor environmental quality [63], and they can be used to trace other contamination in the environment, not only MPs. Moreover, other matrices of the hive, such as pollen and propolis, can be analyzed for contamination of pesticides and other compounds.

Nevertheless, future research must evaluate how plastic pollution impacts on wild species of insects, given that biology, ecology, and genetics are important on the effect of contaminants as well as influence the routes of transmission and levels of exposure. For example, population of solitary insects might be more susceptible than social species, that is honeybees, where the loss of individuals does not pose such a threat to population and can cope better with the toxic compounds of the environment. Furthermore, research needs to focus on potential interactions between MPs and other compounds in field conditions, to better understand how they impact on honeybee and pollinator health. These future studies in field conditions should last longer in order to determine if contamination within hives has any impact on chronic health [47].

The problematic with MPs is difficult to solve, due to the dispersion of pollutants across political borders. For this reason, a global framework must be established that allow countries to collaborate. However, until now environmental regulations are quite permissive about MPs levels of industrial plants [30]. Studies with realistic concentrations of MPs close to those present in the environment are necessary in order to estimate health risks in the environment and in pollinators. Apart from this, it is necessary to use standardized protocols and report results in the same concentration units, since the use of different MPs composition and sizes and shapes across studies makes it difficult to compare them [47].

Extra effort should be implementing of pollinator conservation policies due to their decline could lead to impairment in plant-pollinator biology. This problem has many layers, since pollinators are not only affected by MPs. A holistic and interdisciplinary approach needs to be adopted to deal with the situations that are putting on edge the conservation of pollinators.

9. Final statement

Modern society is confronted with new challenges and issues related to everyday products, which often contain an abundance of plastic polymers in their structure. Despite the limited number of academic publications exploring the potential deleterious effects of NMPs, the experience of recent decades with endocrine disruptors and the current body of evidence should be sufficient to prompt authorities and governments to act. While an outright ban on plastics may be economically challenging in the current context, it is essential to implement actions aimed at environmental health literacy. Associations, institutions, and governments must promote awareness campaigns regarding the ecological impact of plastics and their effects on public health. Additionally, governments should take into consideration the precautionary principle considering current scientific evidence and promote measures to limit the use of plastics, particularly in the context of food.

As a result, environmental health literacy should bring attention to the plastic issue and promote small actions that gradually resonate within society. The goal is to progressively modify people’s lifestyles, leading them toward more sustainable ways of living with reduced plastic usage. Because of the ever-evolving political environment, it is typical for policies and changes to be put into action on a short-term basis. In this sense, the World Health Organization developed the One Health Initiative, an approach that aims to balance and optimize the health of people, animals, and the environment as a whole. In this context, governments, stakeholders, and researchers should work together to manage health threats such as the ones mentioned in this chapter. It is essential to acknowledge that the necessary changes in this case have far-reaching implications for the fabric of society and should be cultivated over the course of generations. The actions we take today will impact the future of humanity.

Acknowledgments

The authors want to thank Elisa Moreno-Mizileanu for her indispensable logistical support.

Conflict of interest

The authors declare no conflict of interest.