A stranger in paradise

25 October 2013 by Malcolm Campbell, posted in Biology

If I stand starry-eyed, that's the danger in paradise.” from Stranger in Paradise by Robert Wright (1914-2005) and George Forrest (1915-1999)

They are harbingers of autumn. Colourful congregations of harlequin ladybirds are a clear indication that fall is upon us. They are a delightful addition to our autumn paradise – a time of vibrant colours, marvellous migrations, and other amazing occurrences as this part of the world transitions from summer to winter.

On a warm day following a cold night, harlequin ladybirds will gather on bright, south-facing surfaces in search of sites to overwinter. The small beetles take in the last days of warmth before their winter’s hibernation. As a sign of the transition from summer to autumn, the aggregation of harlequin ladybirds is about as good as it gets.

The harlequin ladybird, also known as the Hallowe’en ladybug, or the multicoloured Asian lady beetle, Harmonia axyridis, is a remarkable species. Largely solitary and quiescent in the summer months, a frigid night-time temperature followed by a warm day triggers the aggregation response.

The small beetles rely on visual cues to aggregate. They seek out light-coloured structures, like cliff faces, pale-barked tree species, and the sides of buildings- all that contrast with darker surroundings. They also make use of shorter-range visual cues – specifically their own appearance. With their characteristically black-spotted, red- or orange-dome appearance, their gatherings are readily seen when they occur on the pale sites where they prefer to congregate.

Interestingly, in contrast to other insects, there is no evidence yet to suggest that the harlequin ladybird uses long-range air-borne signals – volatile pheromones – as an aggregation signal. If there is any scent-based cue to reinforce congregation, it is merely that which occurs when they come into contact with each other, and, potentially, something perceived in the faeces left behind by past aggregates.

While the annual aggregation of harlequin ladybirds is a remarkable occurrence, the most noteworthy feature of this autumnal indicator is that it isn’t meant to be here.

The harlequin ladybird is an invader. A stranger in our autumn paradise.

The harlequin ladybird was introduced, multiple times, to various locations around the world from its native Asia. It has been introduced as a biocontrol agent – a tool in attempts to reduce aphid feeding on crop plants. It was first introduced to North America in 1916, then many times since then. The little beetle was brought into Europe in 1982, and into South America in 1986. Following all of these introductions the beetle has spread, invading natural landscapes, and displacing native insects, particularly other ladybirds. They have even spread to Africa, a continent where they were not intentionally introduced. Its capacity to spread form sites of introduction has earned the harlequin ladybird the title of “the most invasive ladybird species on Earth”.

The key to the harlequin ladybird’s success is the reason why it was introduced in the first place – it is a voracious eater. Introduced to eat aphids, the harlequin ladybird is a relatively indiscriminate eater, a generalist. Its appetite is not limited to others – it will readily cannibalise its own as well. The capacity of the harlequin to eat other ladybirds, is a key element of its success. It eliminates native species from the competition, clearing the way for its own domination of the ecosystems in which it finds itself.

As if eating the competition were not enough to ensure its success, the harlequin ladybird has more than its appetite in its winning strategy. For example, while a chemical signal does not appear to figure prominently in the harlequin ladybird’s aggregation response, it uses chemical weaponry in its confrontations with others. Harlequin ladybirds produce an alkaloid antibiotic, harmonine, in its circulatory fluid, the haemolymph. Harmonine is an amazing antibiotic, which provides the harlequin ladybird with resistance to a wide variety of deadly microbes. Beyond this, the harlequin ladybird produces over 50 antimicrobial peptides – many more than most insects. These short polymers of amino acids also impair the growth and survival of a vast diversity of microbes.

Together, both harmonine and the antimicrobial peptides represent a formidable defence. They enable the harlequin ladybird to evade diseases that other species cannot. Moreover, harmonine is toxic to some insect species, and provides a chemical defence against predation. Together, harmonine provides harlequin ladybirds with an advantage that other species simply do not have.

Harmonine is not the only advantage that harlequin ladybirds have over the competition. There’s one final crucial advantage. It’s a parasite that lives in the ladybirds.

In addition to having haemolymph full of harmonine, harlequin ladybird haemolymph also harbours a parasite, a microsporidian. This microsporidian parasite is deadly to other ladybirds. Not so with the harlequin ladybird. Somehow the harlequin ladybird keeps the parasite in check. Despite the fact that the haemolymph is chock full of the microsporidian parasites, they do not harm the eggs or larva of the harlequin ladybird, as they would other ladybird species. Consequently, the harlequin is a carrier of death for other species, but not itself.

When it invades, the harlequin carries deadly passengers – the parasites. These parasites are then unleashed amongst the susceptible natives, killing them, and paving the way for the harlequin’s dominance. This is analogous to European human’s arrival in the Americas in the 15th century. European explorers harboured diseases that decimated the indigenous American population, rendering them susceptible to invasion. The harlequin beetle is following a path that has been well-trodden by humans as we have “conquered” various regions of the globe.

Just as we admire the human capacity for exploration, it’s difficult not to admire the harlequin ladybird’s remarkable success in striking out into new regions of the world. In addition to its charismatic autumnal aggregations, the beetle is an ingenuous example of how evolution hones successful generalists – organisms that are able to live off of whatever is available to them, and to contend with whatever pests and pathogens they encounter on this path.

On the other hand, like invading humans, there is something discomforting in the harlequin ladybird’s dominance of places where they simply should not reside. They are emblematic of humanity’s naïveté, or even hubris, when it comes to the manipulation of nature.

In the regions where they have been introduced, harlequin ladybirds have functioned to reduce the impact of aphids on crops. But they have also been noted as an irritating biting insect in the summer months, and have had a negative impact on some crops, notably grapes. Strikingly, harlequin ladybirds have introduced an undesirable flavour, “of peanuts, bell peppers, and/or asparagus”, to white and red wines. Much more importantly, they have displaced native insect species, and changed the dynamics within ecosystems.

It seems a simple thing to merely move an organism to a new place, and expect that only the good things that it does will manifest themselves in this new locale. Perhaps it is a reflection of the eternal optimism of the human species that the expectation is that only good will come from such a move. Of course, it woefully ignores the fact that nature doesn’t work that way. Organisms are complex entities that don’t merely sit in isolation, but instead interact with a myriad of other organisms. The introduction of a new species may have the desired benefit, but will also simultaneously have a ripple effect that impacts other species, sometimes in an entirely deleterious manner.

But here’s the thing, the introduction and subsequent invasion of a species will almost certainly not destroy Nature.

Nature will sort things out. Some species will dominate – perhaps the invader – and some species will falter – perhaps those that have historically resided in that location. Regardless, species will continue to survive. Evolution will sort things out, as it has done for billions of years.  What is a certainty is that things will be different. The paradise that has existed there for millennia will change.

As we move species like the harlequin beetle about the planet, we must ask ourselves, “What level of change are we prepared to accept?”  What is the price of such “strangers in paradise”? Is that a price that we have the right to make Nature pay?

Images: All photographs by Malcolm M. Campbell

References:

Kindlmann P, Ameixa OM & Dixon AF (2011) Ecological effects of invasive alien species on native communities, with particular emphasis on the interactions between aphids and ladybirds. BioControl 56: 469-476

Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science 3: 32

Lombaert E, Guillemaud T, Cornuet JM, Malausa T, Facon B & Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS One 5: e9743

Nalepa CA, Kennedy GG & Brownie C (2005) Role of visual contrast in the alighting behavior of Harmonia axyridis (Coleoptera: Coccinellidae) at overwintering sites. Environmental Entomology 34: 425-431

Pickering G, Lin J, Riesen R, Reynolds A, Brindle I & Soleas G (2004) Influence of Harmonia axyridis on the sensory properties of white and red wine. American Journal of Enology and Viticulture 55: 153-159

Röhrich CR, Ngwa CJ, Wiesner J, Schmidtberg H, Degenkolb T, Kollewe C  & Vilcinskas A (2012) Harmonine, a defence compound from the harlequin ladybird, inhibits mycobacterial growth and demonstrates multi-stage antimalarial activity. Biology Letters 8: 308-311

Sloggett JJ, Magro A, Verheggen FJ, Hemptinne JL, Hutchison WD & Riddick EW (2011) The chemical ecology of Harmonia axyridis. BioControl 56: 643-661

Vilcinskas A, Mukherjee K & Vogel H (2013) Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proceedings of the Royal Society B: Biological Sciences 280: 20122113

Vilcinskas A, Stoecker K, Schmidtberg H, Röhrich CR, & Vogel H (2013) Invasive Harlequin Ladybird Carries Biological Weapons Against Native Competitors. Science 340: 862-863

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