Metallic starlings: a rain of terror

I am a slow learner. Several times in the past few years I have paddled my canoe under a particular sycamore tree in the New River in Radford, Virginia. Each time I do so, I am greeted by large numbers of cormorant poop bombs dropped by the dozens of cormorants that seem to find that particular tree to their liking, and this particular canoeist not to their liking. Fortunately, cormorants have bad aim, but unfortunately it is not that bad.

Daniel Natusch and three other researchers wanted to know how an analogous form of nutrient enrichment from large colonies of nesting Metallic Starlings (Aplonis metallica) affects the nearby ecosystem in a tropical Australian rainforest. They were interested in this question because it was obvious that the ground below the nesting colony trees was basically devoid of vegetation; they describe it as “an open moonscape”, contrasting sharply with the thick rainforest nearby. Other studies have shown that nutrient enrichment from bird guano leads to increased vegetation density – so why is this ecosystem different?


Lockerbie Scrub rainforest, in Cape York Peninsula, Australia, showing colony tree with dead zone (left) and a continuous rainforest (right)



Dan Natusch conducts herpetological research with his son Huxley. Credit: Jessica Lyons













The researchers compared the biological, chemical and physical environment underneath 27 different colony trees to the environment underneath a randomly chosen tree 100-200 meters from the colony tree. As expected, they found very little vegetation near colony trees, in contrast to relatively dense vegetation near the randomly chosen trees.




Vegetation cover (left) and number of live stems (right) in relation to distance from the colony or randomly chosen tree (Point 0 on X-axis).  Negative numbers are downslope and positive numbers are upslope from the tree.


Soil analyses showed that the soils under the colony trees had much higher concentrations of important nutrients. For example, phosphorus levels were more than 30 times greater, and ammonium nitrogen was about four times greater under colony trees than under the randomly chosen trees. The researchers wondered whether these nutrient levels were so high that they were toxic to vegetation. That would account for the dead zone under the colony trees. An alternative hypothesis is that animals (pigs and turkeys in particular) may be attracted to these high nutrient areas under the colonies, and may either kill germinating plants by eating or trampling them.

Feral pigs (Sus scrofa) rooting and trampling under a colony tree. Credit Daniel Natusch

To test both hypotheses, at the beginning of the breeding season the researchers covered a portion of the colony tree region with metal cages (exclosures) that prevented turkeys and pigs from gaining access. They discovered a much greater number of seedlings under the exclosures in comparison to the areas where turkeys and pigs could access the seedlings.

natuschfig7They concluded that nutrient levels were not toxic to seedlings, but that pigs and turkeys were either eating or trampling the seedlings as they emerge. As you can see, the number of exclosure seedlings dropped sharply in July, in part because rainfall declines sharply in June, which leads to high plant mortality, particularly in the unshaded dead zone. But in addition, feral pigs broke into all of the exclosures that summer to access the seedlings and the nutrient-rich soil.

Do these dead zones actually benefit the starlings in any way? One possible advantage is that dead zones prevent snakes from climbing nearby trees and vines to gain access to the nests that are located high in the canopy of the colony tree. However there is good evidence that colony trees suffer high mortality, as 10 of the 27 colony trees died within three years of the study. Trees that fall during the nesting period could lead to the failure of all of the nests within that colony tree.



A scrub python (Morelia amethistina) puts the squeeze on a juvenile Metallic Starling. Credit Daniel Natusch.


Why do we find dead zones beneath colonies of Metallic Starlings, and increased plant growth rate, larger plant size and greater plant diversity beneath the colonies of several other bird colonies? Most previous studies have looked at sea-bird colonies on small islands that have few terrestrial herbivores, so germinating seedlings are relatively undisturbed. This study occurred in a continuous forest in tropical Australia, which harbored a large population of hungry herbivores. These contrasting findings show the important role of environmental context for understanding how ecological interactions will play out. Given that we humans are continually adding nutrients to our environment (through natural bodily function and when we fertilize our fields), we need to carefully consider the biotic and abiotic players in the ecosystem, so we can predict the effects we are having on the environment.

note: the paper that describes this research is from the journal Ecology. The reference is Natusch, D. J. D., Lyons, J. A., Brown, G. P., & Shine, R. (2017). Biotic interactions mediate the influence of bird colonies on vegetation and soil chemistry at aggregation sites. Ecology 98(2): 382-392. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.


Climate change: to bee or not to bee

From the standpoint of how they regulate their body temperature, we can very crudely divide the animal world into ectotherms and endotherms. Ectotherm body temperature is influenced primarily by the external environment, while endotherms maintain a relatively constant body temperature by conserving the heat they generate from the many chemical reactions that occur within their body. This division is crude because there are many, many organisms, including the bee species that is the focus of this tale, that use both approaches.


The mason bee, Osmia iridis, with a color-marking on its thorax. Credit Jessica Forrest


For now, I’m going to make a generalization that it is very difficult to be a small ectotherm in cold climates. After all, small animals can’t have much insulation, and most of the cells belonging to small ectotherms are located near the surface, and subject to the chilling effects of the cold air. Cold cells can’t do much because most chemical reactions that power our small ectotherm need warmth for maximum efficiency.

Perhaps the most common small-ectotherm-in cold-climates approach is to be active only on warm sunny days. This works great, so long as there are sufficient warm sunny days to get on with the business of life (primarily food, sex and not becoming someone else’s dinner). Rumor has it that there was a huge celebration of small-ectotherms-in cold-climates, when they heard about Donald Trump’s election, as they reasoned that global warming was likely to continue, and they might be able to enjoy a more successful life.

Jessica Forrest and Sarah Chisolm wanted to know how rising temperatures would affect the success of the solitary mason bee, Osmia iridis, in cold climates. This bee survives by consuming nectar and pollen gathered from leguminous plants (bean and peas are common legumes), primarily Lathyrus lanszwertii, and Vicia americana. This bee can elevate its body temperature somewhat above air temperature, but its body temperature, and consequent activity levels are nonetheless greatly influenced by air temperature. The researchers reasoned that warmer temperatures would allow the bees to fly more often and gather more nectar and pollen, so they could grow more quickly, reach a larger size and produce more bee babies.

 Co-author Sarah Chisolm observes bees and wasps at the field site at Rocky Mountain Biological Laboratories in Crested Butte, Colorado. Credit Jessica Forrest.
Three Lathyrus lanszwertii flowers. Credit Jessica Forrest.


But there’s a fly in many ointments, or in this case a brood parasitic wasp, Sapyga pumila, which can lay its egg in a nest cell where the bee has just laid its egg. The wasp egg usually hatches first, kills and eats the bee baby, and, adding insult to injury, also eats the pollen that the bee mother has left to provision its (now dead) baby. So if warmer temperature helps the wasp, by giving it more flight time and faster development, perhaps warmer temperatures will actually decrease the bee’s reproductive output.


Sapyga wasp approaches a bee’s nest entrance. Credit Jessica Forrest



Larval Sapyga wasp (center) begins to eat a bee egg (bottom right). Credit Jessica Forrest













So how does this play out?

Forrest and Chisolm marked and released 109 bees over the course of three years, and discovered that these bees, on average, built more nest cells on warmer days. This could indicate that bee reproductive output increases with temperature. But only if all other factors influenced by air temperature are equal.


But all factors influenced by temperature are not equal. As it turns out, Sapygia wasps, the most significant parasite on these bees, are most active at high temperatures as well. So while bees can make more nest cells at high temperatures, they also need to deal with more parasitic wasps.


These bees make more babies when most of their nest cells are not parasitized. Very few offspring are produced when the parasitism rate climbs above 0.5 (50%).


Overall it’s pretty much a wash for the bees. Bees benefit directly from increased nest cell construction at high temperatures, but suffer from the increased rate of parasitism. In contrast, the parasites are more successful at high temperatures. Several other studies of hosts and parasites have shown that the parasites usually benefit from increased temperature more than the hosts, but there are some counterexamples. The authors caution us that forecasting the impact of future warming requires understanding all the factors that can affect population regulation – a daunting challenge. In the meantime our bees may want to cancel their “We love Donald Trump” party, as their enemies appear to be benefiting more than they are from a warmer climate.

Chironomids: the great Icelandic farmers

Ecologists describe plants and algae as producers because, with the help of solar energy, they produce sugar and other complex carbohydrates from carbon dioxide in the process we call photosynthesis. Consumers, such as horses, chironomids and lions, eat producers or other consumers, using the chemical energy in their food’s complex molecules to fuel their own metabolic processes. Without photosynthesis there would be almost no life, as consumers would need to scavenge the organic molecules that happened to be lurking about in the environment.

You’ll notice I slipped in chironomids as consumers, because they are the diminutive heroes of this tale. There are actually more than 10,000 chironomid species, but the ones we are discussing lay their fertilized eggs into lake water where they sink into the sediment and hatch out as larvae. These larvae go through several growth stages, building tubes which serve as their houses during growth and development. Larvae then transform into pupae, which after a few days swim to the surface and metamorphose into winged adults, which mate and produce more fertilized eggs.


Chironomid Larvae. Credit Michael Drake


Larval tubes in sediment. Credit Cristina Herren








We usually think about consumers as having a negative effect on their food and/or prey. If we introduce a herd of sheep into a small pasture, we are confident that the grass will quickly disappear inside of sheep bellies. Similarly, if we introduce a few lions into a pen of sheep, we can be fairly confident that the sheep population will decline. But consumer effects on populations can act in strange and wonderful ways.

The subarctic Lake Mývatn in Iceland is host to an amazingly huge number of chironomid larvae; over 100,000 of these insects can squeeze into 1 m2 of lake bottom!


Lake Myvatn. Credit Michael Drake


Swarming adult chironomids. Credit Michael Drake






As Cristina Herren describes, Lake Mývatn has long been studied because of the dramatic changes in chironomid densities. Chironomid populations can increase 10-fold in each of four or five consecutive generations during the subarctic spring and summer. So if you began with a density of 10 chironomids/m2 in April, you might find 100/m2 in May, 1000/m2 in June, 10,000/m2 in July and 100,000/m2 in August. Herren was intrigued by this exponential growth, as it suggested that somehow chironomid food resources (primarily algae) were keeping pace with the exploding chironomid population, despite being eaten by this ever-expanding population. How could the algae keep pace with the furious chironomid growth rate? Herren wondered whether the chironomids were acting as farmers and somehow stimulating algal production.

Herren worked with several other researchers to figure out the answer to this puzzle. First, they wondered whether the larval tubes provided an awesome place for algae to live. Second, perhaps chironomids were pooping-out vast quantities of nutrient-rich waste products, which algae used to build their bodies. Either or both of these positive effects could more than compensate for the direct negative effect from chironomids eating the algae.

To investigate both hypotheses, the researchers set up 1-liter clear plastic containers with lake sediment and either 0, 50, 100, 200, 400, 600, 800 or 1200 chironomids (that must have been fun to count!). They placed six or seven containers with each population size into racks at the bottom of the lake.

The first task was to discover whether production actually increased with chironomid abundance. Oxygen is a waste product of photosynthesis, so scientists use oxygen production to measure photosynthetic rate, and also to infer algal abundance. They found that oxygen production actually increased with chironomid abundance. Note that chironomids (and the algae too) actually consume oxygen (just like you and I do) in the process of respiration, so this is a truly remarkable result. It indicates that production increased so much that it more than compensated for the oxygen used up by the chironomids and algae from respiration.


The algae use chlorophyll a in their cells as the molecule for photosynthesis, so algal abundance can be estimated by measuring how much chlorophyll a is present in each bottle. Again, they found more chlorophyll a in the bottles with more chironomids, despite the fact that chironomids were eating all the algae they could find.


In addition, the chironomids from more crowded conditions weighed more than those from sparsely-populated bottles. The researchers concluded that by eating algae, the chironomids were actually increasing algal abundance, thereby creating more food for themselves.

These findings fly in the face of our usual assumptions about consumers reducing the population size of the species they are consuming. The researchers confirmed two important indirect effects of chironomids on algae. First, the chironomid larvae do excrete vast quantities of concentrated nutrients (nitrogen and phosphorus) that are consumed by the algae. In addition, the chironomids tubes are indeed ideal surfaces for algae to hang-out on, as evidenced by finding much more chlorophyll a on the tubes than in the nearby sediment.

We citizens need to recognize that both direct and indirect effects operate within ecosystems. In this case, algae are clearly directly benefitting chironomids by providing them with food. Less obvious, the chironomid effects on algae are in two directions. Chironomids have a direct negative effect on algal populations by consuming vast quantities of algae. However, they have a stronger indirect positive effect on algal populations, by providing algae with high quality housing and abundant resources, so that the algal population grows dramatically over the year. The net effect of chironomids on algal populations (dashed arrow) is positive.


Most ecosystems have many different direct and indirect effects operating between a large number of species. It’s a real challenge to identify and understand these diverse interactions, which is why we need to be cautious about changing ecosystems in significant ways. For example, when we dump our waste products into waterways or soils, the added nutrients can have pronounced direct and indirect effects on the species that live there. In many cases, we won’t be able to identify the unintended consequences of our actions on an ecosystem until the native species have gone extinct.

note: the paper that describes this research is from the journal Ecology. The reference is Herren, Cristina M., et al. “Positive feedback between chironomids and algae creates net mutualism between benthic primary consumers and producers.” Ecology 98.2 (2017): 447-455. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.