Tag Archives: Photosynthesis

Ants and acacias: friends, foes or frenemies?

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In his massive elegy, “In Memorium A. H. H.”, Alfred, Lord Tennyson laments the death of his friend, Arthur Henry Hallam, at 22 years old. Tennyson writes,

“Who trusted God was love indeed

And love Creation’s final law

Tho’ Nature, red in tooth and claw

With ravine, shriek’d against his creed”

Thus Tennyson accuses the natural world of being rife with strife and violence.

It would be wrong to dispute Tennyson’s complaint outright, but ecologists can present mutualisms, interactions in which both species benefit, as a counterpoint to his argument. One of the best studied is the ant/acacia tree mutualism, in which acacia trees provide food and living accommodations to ants, which protect their home tree against herbivores, including immense creatures such as elephants and giraffes! Previous research had shown that acacias usually grew better if they harbored a colony of protective ants, even though they were providing the ants with costly resources. These resources included swollen thorns (domatia) which ants may use as homes or fungal gardens, and specialized structures (nectaries) which provide ants with sugar.

Swollen thorns (domatia) on an Acacia drepanolobium tree that is hosting Crematogaster nigriceps ants. Credit: Patrick Milligan.

As an undergraduate at the University of Florida, Patrick Mulligan learned about how ecology could be thought of as the study of the economy of nature.  Keeping with the economic metaphor, Mulligan recognized that the tiny ants and relatively large trees trade in the same currency: carbon. He realized that tree growth is simply a measure of how much carbon a tree has to spend on itself. So he asked if ants might be influencing how much carbon is available for both themselves and the tree.

Acacia drepanolobium, the dominant tree in the savanna. Credit Patrick Milligan.

In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host plants, the dominant woody plant in the savanna (see photo above). These ants differ in several traits including how much protection they actually provide, whether they consume tree-produced nectar, how they modify the tree, and how they influence a tree’s water relations (see photo and table below). If a tree can’t get enough water, it is forced to close the stomata on its leaf surface to reduce water loss from transpiration. When stomata are closed, carbon dioxide import is drastically curtailed, and photosynthetic rates (and carbon production) are reduced.

The four ants species studied by Patrick Milligan and his colleagues are Crematogaster sjostedti, C, mimosae, C. nigriceps and Tetraponera penzigi. Credit: Todd Palmer.

To determine how the four ant species influence carbon fixation and water relations in these acacias, Milligan and his colleagues set up a five-year ant-removal experiment between 2013-2018.  They found 48 matched pairs of trees that harbored each ant species (12 pairs of trees per ant species), and then removed all of the ants from one of the two trees by fogging with a short-lived insecticide. The researchers restricted ant recolonization by applying to the base of each tree an annoyingly sticky substance that ants generally avoid. 

After five years (in 2018), Milligan and his colleagues measured photosynthesis and transpiration rates in leaves of each tree, using tools that were specialized for those purposes.  They then extrapolated from these leaf measurements to photosynthetic and water exchange rates for the entire tree crown (where most of the action is). They discovered that trees with C. mimosae (Cm) and T. penzigi (Tp) had substantially higher photosynthetic rates than trees with C. sjostedti(Cs) and C. nigriceps (Cn).  But trees that had their ants removed were statistically indistinguishable in their photosynthetic rates (graph (a) below). In other words, removing ants caused Cm and Tp-trees to reduce their photosynthetic rates, and Cs and Cn tree to increase their photosynthetic rates, so they were equivalent after five years of ant removal.  

(Graph a) Mean (+SE) photosynthetic rate at the tree crown and (Graph b) transpiration rate at the tree crown for acacia trees with ants present or removed. The letters to the side of each data point indicate when two species have statistically significant differences in their value. For example, in graph a, comparing the case where ants were present, the photosynthetic rates for Cm and Tp are not different from each other, but both are significantly greater than the photosynthetic rates for Cn and Cs. However, Cn and Cs have similar photosynthetic rates.

Looking at the table above, you will note that both Cs and Cn do some major alterations to the trees that might compromise carbon production. Though Tp does remove nectaries, it also consumes no nectar, so that interaction may be a wash. Based on these observations, we might suspect that Cs and Cn are actually tree parasites, while while Cm and Tp are closer to true mutualists that actually benefit the host trees. Supporting this idea, removing Cs sharply increased leaf area and also increased water exchange rate (graph (b) above).  And trees that were continuously occupied by Cn also showed reduced leaf area, lower photosynthetic rates (graph a above) and water exchange rates (graph b above) at the tree crown than Cm or Tp. But there is more to the story.

Cn is an aggressive defender against would-be herbivores.  However, it also eats large portions of the tree it inhabits focusing on the nectaries (which produce sugars) and the reproductive structures.  One puzzling consequence of this behavior is that Cn-occupied trees are significantly better than other ant-occupied trees at bringing up subsurface water, perhaps helping the tree to survive droughts.  The researchers plan to measure the root systems of all the trees in hopes of seeing whether Cn-occupation actually alters root development in a way that improves water uptake.

Complicating the story further is a consideration of carbohydrate production. Trees hosting Cs (the stem excavator) had much less starch in their stems than did trees hosting the other species.  Starch is an important source of energy for all plants; in fact trees with Cs removed still had low starch levels after five years.  Presumably the trees that were freed from hosting Cs prioritized growing new branches, or repairing cavities and defending against beetle infestation, over producing more starch for storage. 

Trees occupied by Cm (a nectar consumer) had much higher glucose levels than trees hosting the other three species.  Removing Cm caused the glucose levels to drop sharply (see graph below). Trees hosting the other nectar consumer (Cn) did not show this increase in glucose, possibly because Cn prunes the leaves and eats the flowers, leaving the host tree with insufficient nutrients to increase glucose levels. 

Mean (+SE) glucose levels in the stems of trees hosting each ant species. Notice the sharp drop in glucose concentration five years after Cm removal.

I asked Patrick Milligan how trees get occupied by a particular ant species.  He responded that there are battles for occupancy both between ant species, and sometimes within ant species.  An ant from one colony locks in a death grip with an ant from another colony, they then fall from a branch and kill each other on the ground.  So the bigger colony wins a battle by virtue of having some surviving ants to colonize the tree. One exception is Cs, which has slightly larger and presumably stronger ants, and will sometimes survive a head-to-head battle. Currently, Milligan and his colleagues are investigating how a tree may adjust its leaf physiology when paired with a new ant species, perhaps by activating different genes in response to the novel species.  Though trees cannot choose their ant colonizers, they may be able to adjust to whichever species uses their services.

note: the paper that describes this research is from the journal Ecology. The reference is Milligan, P.D., Martin, T.A., Pringle, E.G., Prior, K.M. and Palmer, T.M., 2023. Symbiotic ant traits produce differential host‐plant carbon and water dynamics in a multi‐species mutualism. Ecology, 104(1), p.e3880. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Invading hippos

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Jonathan Shurin was studying declining water quality in Lago de Tota, Colombia’s largest lake, when he learned about a local invasion of the common hippopotamus, Hippopotamus amphibius.  Four hippos were imported to Colombia by the notorious drug lord Pablo Escobar to populate his private zoo.  Following Escobar’s shooting death in 1993, the zoo fell into disrepair and the hippos wandered off free.  The population now numbers between 65-80, and breeding individuals have been seen 150 km from the zoo.

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Hippos wallow in a lake framed by cattle egrits. Credit J. Shurin

Common hippos are native to central and southern Africa; as their scientific name implies they divide their existence between land (mostly at night) and water (keeping cool during the day).  These are huge animals, weighing up to 1500 kg and capable of running a surprising 30 kg/hr.  Apparently it is very easy to annoy a hippo.  From an ecosystem standpoint, hippos in their native Africa have been shown to have a strong impact on ecosystems by grazing on land at night and then releasing processed nutrients into lakes during the day.  Their influence is greatest during the dry season when they’re concentrated at high densities.  Jonathan Shurin and his colleagues wanted to know whether hippos were having a discernable effect on lakes and rivers in Colombia.  Given an expectation that the hippo population will continue to grow, this question has important management implications.

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A grazing hippo. Credit: J. Shurin

The researchers sampled 14 small lakes at Hacienda Napoles in Antioquia, Columbia during the wet season and the dry season.  All lakes were sampled from shore because entering a lake containing hippos can be hazardous to a researcher’s health.peligrohippo

Two lakes were found to contain hippos, while the other 12 did not (though some had been observed with hippos on other occasions).  The analysis compared the two lakes with hippos to the 12 lakes without hippos for nutrients, conductivity, pH, temperature and chlorohyll-a concentration (a measure of photosynthetic activity).  The researchers sampled for phytoplankton, zooplankton and used dip nets to sample macroinvertebrates.  They found few differences in most categories except for the composition of the phytoplankton community. As you can see below, lakes with hippos had considerably more cyanophytes (photosynthetic bacteria often associated with harmful algal blooms), and fewer chlorophytes and charophytes (types of green algae) than did lakes without hippos.

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Mean relative density of different divisions of phytoplankton in the two lakes with hippos (left bar) and the 12 lakes without hippos (right bar).

Shurin and his colleagues also estimated net production of each lake by systematically measuring dissolved oxygen concentration throughout the day. Photosynthetic organisms in highly productive lakes should take up lots of carbon dioxide during the day, and release considerable oxygen into the water.  Thus the difference in oxygen levels during the day (when photosynthesis occurs) vs. night (when there is no photosynthetic activity) would be greatest in highly productive lakes. The researchers discovered from multiple samples that the two lakes with hippos had an average range of 3.6 mg/L in dissolved oxygen levels which was significantly greater than the average range of 2.1 mg/L measured in three of the lakes without hippos (it was not feasible to measure all of the no hippo lakes). Presumably, this difference occurs from high photosynthetic rates during the day in the lakes with hippos.

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Time series of dissolved oxygen in the sampled lakes.  Notice how dissolved oxygen levels peak in the late afternoon (hour 12 = noon), but decline overnight without input from photosynthesis.

In addition to comparing the quantity of nutrients, Shurin and his colleagues wanted to know the source of the nutrients.  Stable isotopes are forms of elements (in this case carbon and nitrogen) that differ in number of neutrons.  They are called stable, because they don’t undergo radioactive decay.  Stable isotope analysis measures the ratio of rare isotopes of a particular element in comparison to the more common isotope (for example 13C compared to 12C). Relevant to the hippo study, plants growing on land tend to have a higher (less negative for carbon, more positive for nitrogen) stable isotope ratio of carbon (delta13C) and nitrogen (delta15N) than do plants growing in water.  So if hippos were bringing nutrients into the lakes, the researchers expected the two hippo lakes to have higher stable isotope ratios of carbon and nitrogen.

As you can see from the graph below, on average, the two hippo lakes had higher stable isotope ratios of carbon, but not of nitrogen.  This indicates that hippos are importing carbon into the lake – presumably eating 13C rich plants during the evening, and then pooping out the remains when they return to the water.  However there is no evidence that hippos are importing nitrogen into the lakes.

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Stable C and N isotopic ratios for samples collected from lakes with (green) and without (orange) hippo populations. Solid circles are the mean values of multiple samples collected at different times from the same lake, and open circles are the individual observations from each sample.

Shurin and his colleagues acknowledge the difficulty of drawing conclusions on ecosystem impact based on only two lakes with hippos.  On the other hand, finding significant differences with such a small sample is noteworthy, particularly when considering that the hippo invasion may be in its early stages.  If we extrapolate, from four hippos in 1993 to the lower estimate of 65 hippos at the time of the study, and assume exponential growth, we should find 785 hippos by 2040 and over 7000 hippos by 2060.  There are several assumptions with this extrapolation, but if unchecked the hippo population could expand dramatically, impacting ecosystem functioning in many different ways.

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Observed (solid circles) and projected (open circles) growth of the hippo population in Antioquia, Columbia, assuming exponential growth.

But should we worry about this?  After all, hippos are amazingly cool, and tourists have begun visiting Hacienda Napoles specifically to see the hippos.  This is an example of a social-ecological mismatch, where the societal value placed on a species may oppose potential negative environmental impact. Conservation ecologists will need to work with the local community to devise a plan that serves the best interests of the ecosystem, and the humans who live there.

note: the paper that describes this research is from the journal Ecology. The reference is Shurin, J. B., Aranguren-Riaño, N., Duque Negro, D., Echeverri Lopez, D., Jones, N. T., Laverde‐R, O., Neu, A., and Pedroza Ramos, A. 2020. Ecosystem effects of the world’s largest invasive animal. Ecology 101(5):e02991. 10.1002/ecy.2991. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

Light levels limit lake phytoplankton response to fertilization

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One might naively think that because we humans are land-dwelling creatures, our impact on aquatic ecosystems might be relatively minor. Unfortunately, this assumption is incorrect, as human activities are changing aquatic environments in profound ways that influence how aquatic species survive and interact. Global warming is increasing lake and river temperatures, uncontrolled development is causing some streams to run dry and others to flood, and agricultural practices are adding nutrients to many lakes and streams. Because these human impacts occur simultaneously, it is difficult to evaluate how each factor contributes to the observed changes in species relations.

In northern Sweden, lakes vary naturally in the amount of dissolved organic carbon (DOC) they contain. DOC comes from runoff of decaying plant matter, so lakes surrounded by substantial vegetation, or that experience a great deal of water input (runoff) from the surrounding area, would have higher DOC than other lakes. DOC is potentially very important to lakes, because DOC tends to discolor a lake, which reduces light penetration and slows down photosynthesis. On the positive side, carbon may bond to other molecules such as phosphorus and nitrogen, which are important nutrients that may be in short supply in these relatively infertile lakes.   Anne Deininger and her colleagues focused their studies on two factors: DOC and nitrogen. Most lakes have too much nitrogen, a result of excessive use of nitrogen fertilizers that run off into lakes, so these relatively low-nitrogen lakes provided the researchers with a unique opportunity to see how these two factors, DOC and nitrogen, interacted in a natural ecosystem.

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Low DOC control lake. Credit: M. Klaus

The researchers selected six lakes that varied naturally in DOC levels: two low (~7 mg DOC/liter), two medium (~11 mg DOC/liter), and two high (~20 mg DOC/liter). In 2011 they measured everything possible about each lake: abundance of all of the life forms, DOC, temperature, light levels, nutrients and photosynthetic rates. In 2012 and 2013, they supplemented one of each pair of lakes with nitrogen compounds every one to two weeks. The added nitrogen was equivalent to the higher nitrogen inputs that are experienced by lakes in southern Sweden. And, as you might expect, the researchers continued measuring all factors of interest in both the experimental (fertilized) and control (unfertilized) lakes throughout the year – at least until the lakes froze over.

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Anne Deininger (in orange) and Sonja Prideaux collect samples from a lake. Credit: M. Deininger.

Deininger and her colleagues were most interested in differences in the abundance of phytoplankton – small free-floating photosynthetic organisms, because these are the primary producers – the organisms that produce the chemical energy (via photosynthesis) that enters food webs. There are many different types or groups of these phytoplankton; some are flagellated, with hair-like processes that allow them to navigate in the water column. Some are exclusively autotrophs, producing their own energy from photosynthesis, some are primarily hetrotrophic, eating other organisms or the remains of dead organisms, while others are mixotrophs, using both strategies to produce energy. Cyanobacteria are photosynthetic bacteria, while picophytoplankton are phytoplankton of unusually small size.

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Flagellated phytoplankton (Cryptomonas). Illustration by Anne Deininger.

Many important findings are summarized in the graph below. “B” represents the year before fertilization (2011), while “A1” is 2012 (after fertilization – 1st year) and “A2” is 2013 (after fertilization – 2nd year). Remember only the N-lakes were fertilized; the control lakes were simply monitored all three years. One finding is that in 2011, the high DOC lakes had the lowest phytoplankton abundance.  A second is that the low and medium DOC lakes had both flagellated and non-flagellated phytoplankton, while the high DOC lakes were dominated by flagellated phytoplankton.

Moving to the years after fertilization (A1 and A2), you can see that nitrogen fertilization increased phytoplankton abundance, but more so for the low-DOC lake. However, fertilization had little impact on the types of phytoplankton found in each lake; rather it simply increased the abundance of already existing groups.

DeiningerFig1

Mean biomass of major phytoplankton groups in relation to DOC.  Recall that B refers to 2011 (the year before fertilization), while A1 and A2 refer to the two years after fertilization (2012, 2013).

The data can be organized so we can get a better view of what is happening quantitatively. Fertilization increases phytoplankton biomass, but much more for lakes with low DOC levels. In addition DOC appears to decrease phytoplankton abundance.

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Deininger and her colleagues conclude that in these northern lakes, phytoplankton production is nutrient-limited at low DOC levels, but becomes limited by light availability in more murky waters. So adding nitrogen increases phytoplankton abundance to a greater extent in low DOC lakes. High DOC lakes have more flagellated autotrophs, as these species can swim to the top of the water column where there is more light for photosynthesis. As needed, flagellated phytoplankton can move lower in the water column where nutrients are more abundant.

The researchers emphasize that the nitrogen experiments were only conducted for two years. They don’t know if, for example, the types of species would change if fertilization continued for more than two years. They also don’t know if after 2013, the communities reverted to their pre-fertilization state, or if biomasses remained higher when nitrogen fertilization stopped. These types of questions are important to pursue because we humans are making drastic changes to most of our aquatic systems in a very uncontrolled manner. We need to understand the effects of these changes to the aquatic environment, and also how we can reverse the effects should they prove to be highly detrimental.

note: the paper that describes this research is from the journal Ecology. The reference is Deininger, A., Faithfull, C. L., & Bergström, A. K. (2017). Phytoplankton response to whole lake inorganic N fertilization along a gradient in dissolved organic carbon. Ecology, 98(4), 982-994. 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.

Chironomids: the great Icelandic farmers

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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.

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Chironomid Larvae. Credit Michael Drake

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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!

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Lake Myvatn. Credit Michael Drake

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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.

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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.

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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.

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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.