I met Alexandra Magro this spring, at the first Grand Conference of the French Academy of Sciences entitled “Insects: Friends, Foes, and Models.” I had contributed a presentation of the blog series Silent Spring Continued at the poster session, hoping to attract insect lovers ready to tell me their stories of love and loss. The conference promised to address the key topics of insect biology—from their interaction with the environment, to their use in biomedical and ecological research—yet most papers focused exclusively on insect biology at the molecular level. Alexandra’s interests were much broader. She works at the CNRS Laboratory for Evolution and Biological Diversity in Toulouse, which is part of the LabEx (Laboratory of Excellence) TULIP network.
From genes to ecosystems, the collaboration aims to overcome the confinement of each discipline and promote an integrative approach, combining both biology and ecology. Alexandra is interested in the intricate mechanisms of insect behavior and how they evolved, and wants to understand them in the context of entire ecosystems. She is ready to cross the boundary between disciplines in order to understand, for instance, how ladybird beetles orient themselves in space by drawing on complex chemical cocktails. From researching the mechanisms by which chemical information is received, to the impact that ladybirds using this information might have on their prey, she hopes to contribute to the understanding of the processes that shape ladybird–prey communities. Using ladybirds as a biological model, she is also interested in biological invasions, the evolution of defenses, diapause aggregations, or asexuality. “Some people say that I do too many different things, which could be damaging for my career. They might be right, but I do what I find relevant. I also want to spread the knowledge to lay people. Part of my job as a lecturer is training secondary school teachers, and I also work a lot with children.”
The fine descriptions in old entomological tomes show all the admiration that the researchers had for the insects they were studying. Today the discipline is very fragmented: the time it takes to obtain diplomas is getting shorter, students do less fieldwork, they may have more specialized knowledge but they lack a global understanding of nature.
When I studied at Lisbon University, I was lucky enough to have a fascinating entomology professor, J. A. Quartau, who among others, told us stories about insects as pest-control agents. I wanted to become a biologist and do something useful, in particular I was interested in contributing to a more environmentally friendly agriculture. Biological control, which replaces the use of pesticides, looked like a promising field. But, when I later took on a Masters in Integrated Pest Management, I found myself greatly disappointed. Pest management seemed to be all about simple recipes. I was interested in ladybird beetles (Coccinellidae), which have worked up a good reputation in the realm of pest control. However, although I learned to observe ladybird beetles in orchards, counted them, and described the changes in their numbers over time, I was unable to understand the interactions in the ecosystem that actually lead to what I was observing.
Therefore, during my PhD, I decided to take a closer look at ladybird–prey interactions, and study how these relationships evolved. The first thing I examined were the strategies ladybirds have developed to cope with the constraints imposed on them by their prey. In our temperate climates there are basically two groups of ladybirds that feed on other insects (there are others, too, that are not predators but eat fungi or plant matter). The first group of insectivorous ladybirds feeds on aphids. Among them are the large seven-spot ladybird, (Cocinella septempunctata), the two-spot ladybird (Adalia bipunctata), and the famous harlequin ladybird (Harmonia axyridis) originating from Asia. The second type feeds on coccids, a group of scale insects. Among them are the heather ladybird (Chilocorus bipustulatus) and the introduced, and highly predatory, Australian Cryptolaemus montrouzieri.
The way the two types of prey (aphids and coccids) live is divergent, and so different species of ladybird have specialized on them. Aphids live at a very fast pace: their lifecycles are tuned-in to the peak growth time of plants—a very limited period, mostly in spring—so they have to develop and reproduce fast. If you have a rosebush in your garden or on your balcony, you will notice that aphids are mainly present in April and May, and after that, you don’t see them anymore. In order to get off to a quick start, female aphids in spring are asexual: they reproduce alone, giving rise to all-female offspring. Therefore, they don’t lose any time trying to find a male and performing all the rituals of sexual reproduction. Furthermore, aphids exhibit telescoping generations: that is, a viviparous female already carries “pregnant” daughters inside her: if you examine a gravid female carefully through a good microscope, you can see her granddaughters inside her daughters. This last generation are almost ready to reproduce as soon as they are born!
Some ladybirds have adapted to this fast-paced cycle. In spring, they come out of diapause (a kind of invertebrate hibernation) and lay their eggs on the aphid colonies, on which their larvae feed once hatched. By the time the aphid population has somewhat receded, the ladybird young are reaching the adult stage. If too many ladybird eggs are laid on the same colony of aphids, there won’t be enough to eat. Moreover, if there are already ladybird larvae on the same spot, they might eat the eggs of other ladybirds coming to lay their eggs there. Aphid-eating females therefore prefer to distribute their eggs in multiple, young aphid colonies, in order to increase the chances of their offspring surviving potential starvation or cannibalism. Of course, this is all contrary to the interests of the farmer, who wants the ladybirds to lay as many eggs as possible in the same spot to eradicate the entire aphid colony fast.
The adult ladybirds have adapted to go fast, but the aphids still go faster: for this reason, there are in fact few successful cases of using adult ladybirds for the biological control of aphids. Our knowledge of these cycles means that instead of releasing adult ladybirds to control aphids, we can release their larvae—the problem with this though is that it is only feasible on certain crops, such as those grown in glasshouses.
For the coccids, it is all to the contrary. Without going into the details of this large group’s broad reproductive strategies, one can say that compared to aphids, they are really slow. Their populations start growing in spring and are still developing well into the summer. Sometimes you can even still find them in autumn. So, the ladybirds that depend on coccids as a food source, don’t have to rush, as their lifecycles take a pace almost the same as that of their prey. As a consequence, there is much more success in biological control programs targeting coccids than aphids.
Recently, I became interested in the fascinating fact that some species of ladybirds form overwintering aggregations, which can reach an impressive number of individuals. I wondered what the impacts of this might be for crop protection and ladybird conservation. These aggregations happen every year, at the same sites. One of our PhD students, Eline Susset, showed that these aggregations seem to be part of the ladybirds’ mating system, forming the venue for a kind of speed dating. In spring, at the end of diapause, females leave the aggregation to reach their breeding sites, but Eline showed that in fact, they are almost all already fecund when they leave. These results suggest that the drives to find, and perhaps even choose, mates efficiently, may have been involved in the evolution of overwintering aggregations. This is extremely important, if we want to protect and enhance ladybird populations. Not only must we pay attention to them in their spring and summer habitats, but also in their autumn and winter ones. One of the sites of aggregation that Eline observed was around the pole of a high-tension line next to a crop field. One day, the farmer ploughed the field and soil covered the aggregation, killing all of the individuals. This is one of the paradoxes of agriculture: by destroying the habitats of beneficial insects, like in this example but especially by using pesticides, farmers deprive themselves of the organisms that could be of great help to them.
Biological control of agricultural pests can be achieved in three different ways: control by conservation and enhancement of indigenous beneficial insects, release of beneficial insects produced in biofactories, and by classical biological control by introducing beneficial foreign species. The introduction of an Australian ladybird, Rodolia cardinalis, to California is a well-documented example of successful classical biological control.
At the end of the nineteenth century, Californian citrus plantations were being decimated by a terrible invasive pest from Australia, the cottony cushion scale (Icerya purchase). Farmers were desperate, ready to give up their plantations. This coccid did not cause any problems in Australia and a team of entomologists led by C. V. Riley decided to find out what kept the coccids in check there. One of them, A. Koebele, set sail for Australia and brought back several insect species that were then released in California—among them, R. cardinalis. The result of this was spectacular. The ladybird spread and thrived, reducing the coccid population substantially. Farmers were happy, Koebele was their hero. They presented him with a golden watch. He was considered the savior of Californian agriculture.
Soon after, a second coccid pest of Australian origin, the mealybug Planococcus citri, invaded the citrus plantations and again Koebele was sent to Australia to find their natural enemies. He brought back various bugs, including the ladybird Cryptolaemus montrouzieri, which was successful in reducing the mealybug population. However, there was a problem: it did not survive the Californian winter very well, and had to be reintroduced each spring. This marked the beginning of biofactories; where large quantities of bugs are produced and distributed on an industrial scale.
These two success stories fostered faith in classical biological pest control at the time. Since then, however, we have seen few such successes, probably because, as I mentioned before, there is a lack of knowledge regarding the mechanisms underlying the interactions between predators and their prey. Furthermore, we have become increasingly aware of the problems associated with these introductions. A famous example is the introduction of Harmonia axyridis, an Asian ladybird that has become invasive in America, Europe, and Africa. The spread of this beetle has caused alarm, but there are still few studies on the real impacts of these introductions on indigenous species. H. axyridis can feed on multiple different species of aphids, many of which are not crop pests and can be found in many different habitats.
There are some studies from the Czech Republic and Britain that demonstrate the negative effect of H. axyridis on non-target species, such as indigenous ladybirds, either indirectly by competition for food, or directly because it also predates them. The long-term effects of introduced species on indigenous ones depends on characteristics and attributes of their lifecycles, such as how and to what extent their habitats overlap, and on their prey’s defenses. Ladybirds’ rely on different, species-specific types of toxic alkaloids as their main line of defense. H. axyridis seems to be extremely well defended and has a great capacity to modify the alkaloids of others, rendering them less harmful and allowing it to attack many other species.
My university campus used to be a sort of Coccinellidae supermarket, where I was able to find up to twenty different species of ladybirds. As I know their habitats, I was able to find them easily and even do practical experiments with students on the campus grounds. Since H. axyridis arrived in Toulouse, there are several species I cannot find anymore, or only with great difficulty. Instead, I find large numbers of H. axyridis. I could not write a scientific publication on the basis of this experience, but it is more than a passing impression. Some Belgian colleagues told me that the communities of indigenous ladybirds do recover after a certain time, and I can only hope that that they are right.