Beautiful buds beset bumblebees with bad bugs

Sexual liaisons can be difficult to achieve without some type of purposeful motion.  Flowering plants, which are rooted to the ground, are particularly challenged to bring the male close enough to the female to have sex.  One awesome adaptation is pollen, technically the male gametophyte –  or gamete (sperm)-generating plant. These tiny males get to females either by floating through the air, or by being transferred by animal pollinators such as bees. Plants can lure bees to their flowers by producing nectar – a sugar rich fluid – which bees lap up and use as a carbohydrate source.  While nectaring, bees also collect pollen, either intentionally or inadvertently, which provides them with essential proteins. When bees travel to the next flower, they may inadvertently drop some of their pollen load near the female gametophyte – in this case a tiny egg-generating plant (though tiny, the female gametophyte is considerably larger than is the male gametophyte).  We call this process of “tiny boy meets tiny girl” pollination. Once the two gametophytes meet, the pollen produces one or more sperm, which it uses to fertilize an egg within the female gametophyte.  There is more to it, but this will hopefully clarify the difference between pollination and fertilization.

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Bumblebee forages on beebalm, Monarda didyma. Credit: Jonathan Giacomini.

All of this business takes place within the friendly confines of the flower.  The same flower may be visited by many different bees of many different species. While feeding, bees carry on other bodily functions, including defecation.  They are not careful about where they defecate; consequently a bee’s breakfast might also include feces from a previous bee visitor. Bumblebee (Bombus impatiens) feces carries many disease organisms, including the gut parasite Crithidia bombi, which can reduce learning, decrease colony reproduction and impair a queen’s ability to found new colonies. Because pollinators are so critical in ecosystems, Lynn Adler and her colleagues wondered whether certain types of flowers were better vectors for harboring and transmitting Crithidia bombi to other bumblebees.

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Bumblebee forages on the snapdragon, Antirrhinum majus. Credit: Jonathan Giacomini.

The researchers chose 14 different flowering plant species, allowing uninfected bumblebees to forage on inflorescences (clusters of flowers) inoculated with a measured amount of Crithidia bombi parasites.  The bees were reared for seven days after exposure, and then were assessed for whether they had picked up the infection from their foraging experience, and if so, how intense the infection was. The researchers dissected each tested bee and counted the number of Crithidia cells within the gut.

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Researcher conducts foraging trial with Lobelia siphilitica inflorescence. Credit: Jonathan Giacomini.

Adler and her colleagues discovered that some plant species caused a much higher pathogen count (mean number of infected cells in the bee gut) than did other plant species.  For example bees that foraged on Asclepias incarnata (ASC) had four times as many pathogens, on average, than did bees that foraged on Digitalis purpurea (DIG) (top graph below). Bees foraging on Asclepias were much more likely to get infected (had greater susceptibility) than bees that foraged on several other species, most notably Linaria vulgaris (LIN) and Eupatorium perfoliatum (EUP) (middle graph). Lastly, if we limit our consideration to infected bees, the mean intensity of the infection was much greater for bees foraging on some species, such as Asclepias and Monarda didyma (MON) than on others, such as Digitalis and Antirrhinum majus (ANT) (bottom graph).

AdlerFig1

(Top graph) Mean number of Crithidia (2 microliter gut sample) hosted by bees after foraging on one of 14 different flowering plant species. This graph includes both infected and uninfected bees. (Middle graph) Susceptibility – the proportion of bees infected – after foraging trials on different plant species. (Bottom graph) Intensity of infection – Mean number of Crithidia for infected bees only. The capital letters below the graph are the first three letters of the plant genus. Numbers in bars are sample size.  Error bars indicate 1 standard error.

It would be impossible to repeat this experiment on the 369,000 known species of flowering plants (with many more still to be identified).  So Adler and her colleagues really wanted to know whether there were some flower characteristics or traits associated with plant species that served as the best vectors of disease.  The researchers measured and counted variables associated with the flowers, such as the size and shape of the corolla, the number of open flowers and the number of reproductive structures (flowers, flower buds and fruits) per inflorescence.

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Flower traits measured by Adler and colleagues (example for blue lobelia, Lobelia siphilitica). CL is corolla length. CW is corolla width. PL is petal length. PW is petal width. Credit: Melissa Ha.

The researchers also wanted to know whether any variables associated with the bees, such as bee size and bee behavior, would predict how likely it was that a bee would get infected.  Surprisingly, the number of reproductive structures per inflorescence stood out as the most important variable. In addition, smaller bees were somewhat more likely to get infected than larger bees, and bees that foraged for a longer time period were more prone to infection.

AdlerFig2

Mean susceptibility of bees to Crithidia infection after foraging on 14 different flowering plant species, in relation to the number of reproductive structures (flowers, buds and fruits) per inflorescence.

These findings are both surprising and exciting. Adler and her colleagues were surprised to find such big differences in the ability of plant species to transmit disease.  In addition, they were puzzled about the importance of number of reproductive structures per inflorescence.  At this point, they don’t have a favorite hypothesis for its overriding importance, speculating that some unmeasured aspect of floral architecture influencing disease transmission might be related to the number of reproductive structures per inflorescence.

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Bumblebee forages on Penstemon digitalis. In addition to the open flowers, note the large number of unopened buds.  Each of these counted as a reproductive structure for the graph above. Credit: Jonathan Giacomini.

The world is losing pollinators at a rapid rate, and there are concerns that if present trends continue, there may not be enough pollinators to pollinate flowers of some of our most important food crops. Disease is implicated in many of these declines, so it behooves us to understand how plants can serve as vectors of diseases that affect pollinators. Identifying floral traits that influence disease transmission could guide the creation of pollinator-friendly habitats within plant communities, and help to maintain diverse pollinator communities within the world’s ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Adler, L. S., Michaud, K. M., Ellner, S. P., McArt, S. H., Stevenson, P. C. and Irwin, R. E. (2018), Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees. Ecology, 99: 2535-2545. doi:10.1002/ecy.2503. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Dinoflagellates deter copepod consumption

Those of us who enjoy eating seafood are dismayed by the dreaded red tide, which renders some of our favorite prey toxic to us.  A red tide occurs when dinoflagellates and other algae increase sharply in abundance, often in response to upwelling of nutrients from the ocean floor.  Many of these dinoflagellates are red or brownish-red in color, so large numbers of them floating on or near the surface give the ocean its characteristic red color. These dinoflagellates produce toxic compounds (in particular neurotoxins) that pass through the food web, ultimately contaminating fish, molluscs and many other groups of species.

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Red tide at Isahaya Bay, Japan.  Credit: Marufish/Flickr.

Did toxicity arise in dinoflagellates to protect them from being eaten by predators – in particular by voracious copepods?  The problem with this hypothesis is that copepods eat an entire dinoflagellate.  Let’s imagine a dinoflagellate with a mutation that produces a toxic substance. At some point the dinoflagellate gets eaten, and the poor copepod consumer is exposed to the toxin.  Maybe it dies and maybe it lives, but the important result is that the dinoflagellate dies, and its mutant genes are gone forever, along with the toxic trait. The only way toxicity will benefit the dinoflagellate individual, and thus spread throughout the dinoflagellate population, is if it increases the survival/reproductive success of individuals with the toxic trait. This can occur if copepods have some mechanism for detecting toxic dinoflagellates, and are therefore less likely to eat them.

Jiayi Xu and Thomas Kiørboe went looking for such a mechanism using 13 different species or strains of dinoflagellates that were presented to the copepod Temora longicornis. This copepod beats its legs to create an ocean current that moves water, and presumably dinoflagellates, in its direction, which it then eats.  For their experiment, the researchers glued a hair to the dorsal surface of an individual copepod (very carefully), and they then attached the other side of the hair to a capillary tube, which was controlled by a micromanipulator. They placed these copepods into small aquaria, where the copepods continued to beat their legs, eat and engage in other bodily functions.

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Aquarium with tethered copepod and recording equipment: Credit: J. Xu.

The researchers then added a measured amount of one type of dinoflagellate into the aquarium, and using high resolution videography, watched the copepods feed over the next 24 hours.

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Tethered copepod beats its legs to attract a dinoflagellate (round blue circular cell). Credit: J. Xu.

Twelve of the dinoflegellate strains were known to be toxic, though they had several different types of poison. Protoceratium reticulatum was a nontoxic control species of dinoflagellate.  As you can see below, on average, copepods ate more of the nontoxic P. reticulatum than they did of any of the toxic species.

XuFig1

Average dinoflagellate biomass ingested by the tethered copepods.  P. reticulatum  is the nontoxic control.  Error bars are 1 SE.

Xu and Kiørboe identified two major mechanisms that underlie selectivity by the copepod predator.  In many cases, the copepod successfully captured the prey, but then rejected it (top graph below). For one strain of A. tamarense prey, and a lesser extent for K. brevis prey, the predator simply fed less as a consequence of reducing the proportion of time that it beat its feeding legs (bottom graph below).

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Copepod feeding behavior on 13 dinoflagellate prey species.  Top graph is fraction of dinoflagellates rejected, while bottom graph is the proportion of time the copepods beats its feeding legs in the presence of a particular species/strain of dinoflagellate.  

If you look at the very first graph in this post, which shows the average dinoflagellate biomass consumed, you will note that both strains of K. brevis (K8 and K9) are eaten very sparingly.  The graphs just above show that the copepod rejects some K. brevis that it captures, and beats its legs a bit less often when presented with K. brevis. However, the rejection increase and leg beating decreases are not sufficient to account for the tremendous reduction in consumption. So something else must be going on.  The researchers suspect that the copepod can identify K. breviscells from a distance, presumably through olfaction, and decide not to capture them. This mechanism warrants further exploration.

One surprising finding of this study is that the copepod responds differently to one strain of the same species (A. tamarense) than it does to the other strains.  Xu and Kiorbe point out that previous studies of copepod/dinoflagellate interactions have identified other surprises.  For example, there are cases where a dinoflagellate strain is toxic to one strain of copepod, but harmless to another copepod strain of the same species. Also, within a dinoflagellate species, one strain may have a very different distribution of toxins than does a second strain.  So why does this degree of variation exist in this system?

The researchers argue that there may be an evolutionary arms race between copepods and dinoflagellates.  The copepod adapts to the toxin of co-occurring dinoflagellates, becoming resistant to the toxin. This selects for dinoflagellates that produce a novel toxin that the copepod is sensitive to. Over time, the copepod evolves resistance to the second toxin as well, and so on… Because masses of ocean water and populations of both groups are constantly mixing, different species and strains are exposed to novel environments with high frequency. Evolution happens.

note: the paper that describes this research is from the journal Ecology. The reference is Xu, J. and Kiørboe, T. (2018), Toxic dinoflagellates produce true grazer deterrents. Ecology, 99: 2240-2249. doi:10.1002/ecy.2479. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Meandering meerkats

Dispersal – the movement of individuals to a new location – is a complex process that ecologists divide into three stages: emigration (leaving the group), transience through an unfamiliar landscape, and settlement in a suitable habitat. Dispersal is fraught with danger, as dispersers usually have a higher chance of starving, of getting eaten by predators, and may suffer a low reproductive rate.  So why move?

The problem is that there are major issues with not moving.  First, if nobody disperses, population densities could increase alarmingly, putting strains on resources and increasing the incidence of disease transmission.  Second, if nobody disperses, close relatives would tend to live near each other.  If these relatives mate, there would be a high probability of bad combinations of genes being expressed, leading to developmental abnormalities or high offspring mortality (geneticists call this inbreeding depression). In social species, such as meerkats, Suricata suricatta, the issues are even more complex, as dispersal could break up social groups that work well together to detect predators or find resources.  Nino Maag and his colleagues explored what factors influence meerkat dispersal decisions, their survival and reproduction, and how those factors affected overall population dynamics in the Kuruman River Reserve in South Africa.

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A group of vigilant meerkats. Credit: Arpat Azgul

Meerkats live in groups of 2-50 individuals, with a dominant pair that monopolizes reproduction.  While pregnant, the dominant female usually evicts some subordinate females from the group; this coalition of evictees will either remain apart from the group (but within the confines of the territory) and eventually be allowed back in, or else emigrate to a new territory. By attaching radio collars to subordinate females, the researchers were able to follow emigrants to determine their fates.

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Nino Maag collects data in the Kalahari Desert while a meerkat, wearing a radio collar, strolls by. Credit: Gabriele Cozzi.

How does population density affect emigration rates of evicted females?  You might think that meerkats would be most likely to emigrate at high population density, as a way of avoiding resource competition.  As it turns out the story is more complicated.  First, individual females (solid lines in graph below) are more likely to remain with the group (not emigrate) than are groups of two or more females (dashed lines). Second, emigration rates were highest at low population density, intermediate at high population density and lowest at intermediate population density. This nonlinear effect can be explained by low benefits of remaining in a very small group, so evictees are more likely to emigrate.  But as population density (and group size) increase, then the meerkats enjoy higher success as a result of cooperation between individuals  (in particular, detecting and avoiding predators).  But when population densities get too high, there are not enough resources to go around, and evictees are more likely to emigrate.

MaagFig2A

Proportion of evicted female meerkats that had not yet emigrated in relation to time since eviction at low (red), medium (light blue) and high (dark blue) population density.  Solid lines represent individual females, while dashed lines are coalitions of two or more females.

In addition to the density effects we just discussed, association with unrelated males from other groups early after eviction increased the probability that females would emigrate – presumably this increased the probability females would quickly create offspring in their new territory. Females also dispersed longer distances if unrelated males did not meet up with them, possibly to avoid inbreeding with closely-related males from neighboring groups.

Coalitions were more likely to return to the group if females were not pregnant – in fact 62% of pregnant evictees aborted their litters before being allowed back into the group.  Of the ones that did not abort before returning, only 42% of their litters survived to the first month.

The period of transience, when emigrators are seeking new territories can be prolonged and dangerous.  The mean dispersal distance was 2.24 km, and averaged about 46 days.  Larger coalitions with males present tended to disperse the shortest distances (left graph below). Dispersers took longest to settle at high population density – perhaps there were fewer available territories under those conditions (right graph below).

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A. Effect of coalition size and presence of unrelated males on dispersal distance. B. Effect of population density on transience time (interval between emigration and settling).

Large coalitions settled more quickly than did small coalitions, particularly if accompanied by unrelated males.  Once settled, females successfully carried through 89% of their pregnancies (compare that to the 62% abortion rate of females that returned to their original group).  These females had a litter survival rate (to the first month) of 65%.

Social and non-social species are influenced by population density in different ways.  The situation is relatively simple for non-social species; as population size increases, competition between individuals increases, so dispersal is more likely.  However, even for non-social species, we might expect dispersal at very low population levels, if there are no mates available. For social species such as meerkats, the situation is more complex.  Cooperation enhances survival and reproduction, so it is better to be in a larger group (with more cooperators). At the same time, if the group is too large, then resource competition starts being an increasingly disruptive factor. As ecologists collect more dispersal data from other social species, they will be able to test the hypothesis that population density in many species influences dispersal in a non-linear way.

note: the paper that describes this research is from the journal Ecology. The reference is Maag, N. , Cozzi, G. , Clutton‐Brock, T. and Ozgul, A. (2018), Density‐dependent dispersal strategies in a cooperative breeder. Ecology, 99: 1932-1941. doi:10.1002/ecy.2433. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Intertidal tussles: a shifting balance

As an omnivore with a research-oriented palate, I delight in consuming many different food types.  High on my list are crustaceans – in particular the American lobster, Homarus americanus.

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A juvenile American lobster, Homarus americanus. Credit: C. Baillie.

However, another crustacean, the invasive Asian shore crab, Hemigrapsus sanguineus, threatens to disrupt my epicurean delight, by interfering with the growth and development of juvenile lobsters in the low intertidal zone in the north Atlantic. Christopher Baillie and Jonathan Grabowski have explored interactions between these lobsters and crabs to unravel how they might be influencing each other.

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The invasive Asian shore crab, Hemigrapsus sanguineus. Credit: Rhode Island Marine and Estuarine Invasive Species Site.

The Asian shore crab was first detected off the New Jersey coast in 1988 and quickly spread from North Carolina to Maine. Their increase has coincided with a sharp decrease in the abundance of their rival green crabs over the same range. Baillie and Grabowski were concerned that the Asian shore crab could also be adversely affecting lobster populations. They did monthly surveys (May-October) of both lobster and crab densities in Dorothy Cove in Masachusetts, USA, between 2013 and 2017, and discovered that crab populations were increasing sharply at the same time that lobster populations were decreasing steadily.

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Annual average densities of Asian shore crabs (dark gray) and American lobsters (light gray) from surveys at Dorothy Cove, Nahant, Massachusetts, USA, between 2013 and 2017. Error bars are 1 standard error.

The researchers wanted to know whether the increased number of Asian shore crabs was responsible for the lobster decline. Perhaps the two species competed with each other for shelter. Baillie and Grabowski set up experimental tanks, each containing a wire mesh bottom with a rectangular opening cut in the center, so that a burrow could be excavated.  They then introduced a single lobster or crab to the tank, and allowed it to dig a burrow in the cutout center (we’ll call this individual the resident).

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In one shelter experiment, the researchers compared the behavior of larger (mean carapace length = 24.7 cm) and smaller (mean carapace length = 9.3 cm) juvenile lobsters in the presence and absence of a variable number of crabs. They discovered that both larger and smaller lobsters spent most of the time in their burrow when no crabs were in the tank. However, introducing crabs was a major disruptor to their mellow existence, with both lobster size classes being more likely to abandon their residences when crabs were present.

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Mean (+ standard error) percentage of time spent in shelter by large juvenile lobsters (top graph) and small juvenile lobsters (bottom graph) in relation to absence (Control) or presence of different numbers of crabs.  Different letters above the bars indicate that the means are statistically different from each other.

The reasons for the decline in residence time were very different for large vs. small lobsters.  In an experiment with one large lobster pitted against one crab, resident lobsters initiated an average of 18.00 attacks against crabs, while resident crabs initiated an average of only 0.20 attacks against lobsters. Even if crabs were allowed to establish residency, when a lobster was introduced, it usually picked a fight with the resident crab. So large resident lobsters left their burrows to challenge intruding crabs. Lobsters managed to kill and eat two intruding crabs.

In contrast, smaller lobsters had a much different experience. Crabs attacked resident small lobsters and were able to displace them from their burrow. This was particularly the case when a greater number of crabs were added to the tank.  When eight crabs were added, the poor lobster was kicked out of its burrow, on average, almost 20 times within a six-hour trial.  Under these conditions, crabs attacked the resident lobster almost 40 times per trial.

BaillieFig4

Crab behavior towards a resident lobster in relation to the number of crabs (heterospecific competitors) introduced into the tank. (A) Mean number of times the lobster is displaced. (B) Mean number of fights initiated by an intruder crab. Error bars are 1 standard error. Different letters above the bars indicate that the means are statistically different from each other.

Baillie and Grabowski also conducted feeding trials – but only with a larger lobster pitted against an individual crab (a blue mussel – a preferred food item for both species – was the prey).  Lobsters were much more successful feeders than crabs, and actually increased their feeding rates in the presence of crabs, presumably having no interest in sharing the mussel with its competitor. Taken together, the shelter and feeding experiments suggest a reversal in dominance structure occurs over the course of lobster development.  The abundant Asian shore crab outcompetes small juvenile lobsters for shelter, but once lobsters attain a certain size, they can outcompete crabs for both shelter and food. We still don’t know, for sure, whether the decline in lobsters in the low intertidal zone at the study site was caused by the increase in crabs; the Asian shore crab may still be expanding its range, so it may be possible to more directly study changes in distribution at other sites both north and south of its current range. Fortunately for lobsters (and for lobster consumers), juveniles can also grow and flourish in deeper ocean waters, where Asian shore crabs are much less of a threat.

note: the paper that describes this research is from the journal Ecology. The reference is Baillie, C. J. and Grabowski, J. H. (2018), Competitive and agonistic interactions between the invasive Asian shore crab and juvenile American lobster. Ecology, 99: 2067-2079. doi:10.1002/ecy.2432. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Eavesdropping on antshrikes

Growing up in the Spy vs. Spy era, and a bit later in the Watergate age, I developed a keen appreciation for clandestine operations, which I assumed at that time were unique to human culture.  As it turns out, eavesdropping is practiced by many different species for a variety of reasons. One important example occurs in bird flocks composed of several species of birds. Antshrikes (Thamnomanes ardesiacus) are sentinel species in multi-species flocks because they produce alarm calls when they spot a predacious raptor flying overhead, alerting other nearby birds of the threat. Ari Martinez and his colleagues wondered whether hanging out with antshrikes allowed these other bird species to expand their niches to forage in areas that might otherwise be too dangerous.

Alarm calling species Thamnomanes ardesiacus Photo cred E. Parra 600dpi (1)

An antshrike perched in the Amazonian rainforest. Credit: E. Parra.

This fear-based niche shift hypothesis makes two related predictions.  First, in the absence of antshrikes, the remainder of the flock should shift its range to areas with lower predation risk.  Second, without antshrikes some birds might leave the flock entirely, because without sentinel services they no longer benefit from hanging with other birds. To test these predictions, Martinez and his colleagues identified eight flocks of 5-8 species (including antshrikes) in a tropical lowland forest in southeastern Peru.  They established four removal flocks from which they removed all antshrikes after capturing them in mist nets. They left four control flocks, in which they captured all antshrikes, but then returned them to the flock (to control for the effects of handling).

Group banding and mist netting birds photo ced Micah Reigner

Research team mist-netting and measuring antshrikes.  Credit Micah Reigner

To determine where the flock was spending its time, researchers used a GPS device every 10 minutes to record the center of the flock. They also censused each flock for species composition from dawn to dusk for three days before removal and three days after removal. In control flocks, home range overlapped extensively (average of 69%) when comparing the first (pre-removal) and second (post-removal) three-day period. In removal flocks, there was only 8% overlap in home range, indicating that the remaining flock was shifting its range when antshrikes were gone.

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Home ranges of a control flock (top) and a flock which had antshrikes removed (bottom). Red color indicates home range during the three day pre-removal period, while blue color indicates home range during the three day post-removal period.  Deeper colors indicate greater occupancy. 

But are the remaining species shifting their niches to safer locations when antshrikes are no longer available as sentinels? To answer this question the researchers measured the presence or absence of vegetation cover at different height intervals every 10 minutes at the center of the flock. Comparing the second (post-removal) to the first (pre-removal) period, the removal flocks (those without antshrikes) moved into understory vegetation (0-8 meters high) that was substantially denser than was the vegetation inhabited by the control flocks (those with antshrikes). Presumably, dense understory protects birds without sentinels from being spotted or captured by raptors flying overhead. These dense understory areas are usually associated with less tree cover at higher height intervals (above 16 meters), which allows more sunlight to reach the forest floor, resulting in lush vegetation growth.

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Proportion change in vegetation cover occupied by flocks from pre-trial to post-trial period at different height intervals.  Positive numbers indicate an increase in vegetation density. Error bars are 95% confidence intervals. Data are based on the behavior of four control and four removal flocks.

Flocking occurrence is the proportion of time individuals of a particular species spend in flocks.  The fear-based niche shift hypothesis predicts that flocking occurrence should decrease when sentinel species are removed because the benefits of flocking are reduced for the remaining species. When the researchers compared post-removal to pre-removal time-periods, five species showed strong reductions in flocking occurrence for removal flocks in comparison to control flocks, two were unchanged, and one species showed an increase in flocking occurence.

MartinezFig2

Change in proportion flocking occurrence for eight different flocking species in control and removal flocks.  Error bars are 95% confidence intervals.  Chlorothraupis carmioli (CHCA), Epinecrophylla erythrura (EPER), Epinecrophylla leucophthalma (EPLE), Glyphorynchus sprirus (GLSP), Hylophilus ochraceiceps (HYOC), Myrmotherula longipennis (MYLO), Myrmotherula menetriesii (MYME), Xiphorhynchus elegans (XIEL).

The authors emphasize that though flocking occurrence decreased for most species, the flocks did remain intact, which indicates that there are probably other benefits from flocking besides the opportunity to eavesdrop. There might be safety in numbers – a decrease in individual mortality as group size increases, or the possibility that the remaining flock members do provide some information about imminent predator attacks.

Martinez and his colleagues conclude that sentinels help other bird species succeed in tropical rainforests, thriving in dangerous habitats where they might otherwise fear to tread.  These species may provide important ecosystem services, such as dispersing seeds and eating herbivorous insects that threaten plants that are the foundation of these tropical ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Martínez, A. E., Parra, E. , Muellerklein, O. and Vredenburg, V. T. (2018), Fear‐based niche shifts in neotropical birds. Ecology, 99: 1338-1346. doi:10.1002/ecy.2217. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

 

Parrotfish put on their big boy pants

While it would be awesome if parrotfish were named for their conversational abilities, it turns out that they earn their moniker for their specialized teeth that are fused together for scraping algae from coral, thus resembling a parrot’s beak. Despite lacking verbal skills these fish are incredible. Approximately 100 species occupy reefs, rocky coastlines and eelgrass meadows in tropical and subtropical waters. Many species are sequential hermaphrodites, beginning life as females and then changing into males after reaching a certain size. While female reproductive success is limited by the number of eggs she can produce, male reproductive success can be much higher if he can fertilize the eggs of many females.  So if a parrotfish transitions into a large male, and can control access to numerous females, he will enjoy greater reproductive success than if he had remained a female.

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Two Chlorurus spilurus parrotfish show off their teeth and colors.  The large colorful fish on the right is a male, while the smaller darker fish to his left is a female. Credit: Brett Taylor.

Phenotypic plasticity describes the ability of an individual with a particular genetic makeup to vary in a variety of traits (such as what it looks like, or how it behaves) in response to different environmental conditions. About 15 years ago, Nick Gust’s PhD research on tropical reef fish revealed that tremendous variation in parrotfish traits existed over a distance of a few kilometers. But what causes this variation? When funding became available, Brett Taylor jumped at the opportunity to pinpoint the causes, focusing on the diverse parrotfish community in the Great Barrier Reef (GBR).

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Eastern slope of the Great Barrier Reef hosts a diversity of fish and coral species. Credit: Brett Taylor.

Taylor and his colleagues surveyed 82 sites within 31 reefs across 6 degrees of latitude in the northern GBR. To standardize data collection, divers, armed with a multitude of cameras and GPS devices, swam at a standardized rate (about 20 meters/minute) for 40 minutes per survey, recording each parrotfish along a 5 m wide swath. They collected data about the habitat and the environment, about the physical traits of each individual parrotfish (such as size and sex), and about the type and abundance of parrotfish and their predators present at each site.

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Researcher takes notes while conducting a dive.  Credit Kendra Taylor.

The researchers wanted to identify what factors influenced growth rate, maximum body size, and the size at sex change, and how these factors related to the parrotfish mating system. Four species of parrotfish were sufficiently abundant across the GBR to allow researchers to do this type of analysis.

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Four parrotfish species  abundant along exposed outer shelf (yellow sites) and protected inner shelf (blue) regions of the Great Barrier Reef. Males are larger and more colorful.

The GBR varies structurally across a relatively small spatial scale of 40 – 100 km, with outer shelf regions (eastern) exposed to wave action, and inner shelf regions (western) relatively protected. All four species tended to change sex at a larger size in protected sites than they did at exposed sites. However, the differences are only compelling for two of the species: C. spilurus and S. frenatus. There were fewer data points for the other two species, so it is possible (but unknown) that they too would show a more pronounced trend if more data were available.

TaylorFig1bottom

Proportion terminal phase (sex-changed males) in relation to body size (measured to the fork of the tail) in exposed (yellow) and sheltered (blue) sites.

Not surprisingly, parrotfish grew larger in protected areas. Presumably, less wave action provided a more benign environment for rapid growth, both of parrotfish and their preferred food items (algae growing on rocks and coral).

TaylorFig2I

Standardized maximum size (Lmax) attained by parrotfish in sheltered vs. exposed sites.

The researchers were somewhat surprised that most other factors, such as latitude, coral cover, sea surface temperature, and predator abundance, had very little effect on the size at sex change. Rather, the size at sex change appears to be strongly influenced by the local size distribution. In protected habitats, parrotfish grow large and change sex at a large size, while in exposed habitats, parrotfish are smaller, and change sex at a smaller size.

But sex is never simple. Nick Gust’s PhD research showed that C. spilurus had different patterns of sexual allocation in protected vs. exposed areas. In protected areas, the mating system is haremic, with a large male defending a territory and servicing a harem of females. In exposed areas, the mating system is mixed; there still are large territorial males with their harems, but they compete with many more small males, and group spawning is much more prevalent. Theoretically, the presence of these small males may make it less worthwhile for a female to transition into a male, and may influence the optimal size for transitioning in exposed reefs. Given that we still don’t know the mating system details of the other parrotfish in this study, it will be fascinating to see if they too show similar patterns of haremic vs. mixed mating systems in relation to habitat structure.

note: the paper that describes this research is from the journal Ecology. The reference is Taylor, B. M., Brandl, S. J., Kapur, M., Robbins, W. D., Johnson, G., Huveneers, C., Renaud, P. and Choat, J. H. (2018), Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes. Ecology 99(3): 642-651. doi:10.1002/ecy.2127. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Prey populations: the only thing to fear is fear itself

In reference to the Great Depression, Franklin Delano Roosevelt is famously quoted as stating during his 1933 inaugural speech “the only thing we have to fear is fear itself.” Roosevelt was no biologist, but his words could equally apply to a different type of depression – the decline of animal populations that can be caused by fear.

FDR

Roosevelt’s inauguration in 1933. Credit: Architect of the Capitol.

Ecologists have long known that predators can depress prey populations by killing substantial numbers of their prey. But only in the past two decades or so have they realized that predators can, simply by their presence, cause prey populations to go into decline. There are many different ways this can happen, but, in general, a predation threat sensed by a prey organism can interfere with its feeding behavior, causing it to grow more slowly, or to starve to death. As one example, elk populations declined after wolves were introduced to Yellowstone National Park. There are many factors associated with this decline, but one factor is fear of predators causes elk to spend more time scanning and less time foraging. Also, elk tend to stay away from wolf hotspots, which are often places with good elk forage.

Liana Zanette recognized that ecologists had not considered whether predator presence can cause bird or mammal parents to reduce the amount of provisioning they provide to dependent offspring, thereby reducing offspring growth and survival, and slowing down population growth. For many years, she and her colleagues have studied the Song Sparrow, Melospiza melodia, on several small Gulf Islands in British Columbia, Canada. In an early study, she showed that playbacks of predator calls reduced parental provisioning by 26%, resulting in a 40% reduction in the estimated number of nestlings that fledged (left the nest). But, as she points out, Song Sparrow parents provision their offspring for many days after fledging; she wondered whether continued perception of a predation threat during this later time period further decreased offspring survival and ultimately population growth.

Song sparrow

The Song Sparrow, Melospiza melodia. Credit: Free Software Foundation.

Zanette’s student, Blair Dudeck, did much of the fieldwork for this study. The researchers captured nestlings six days after hatching , weighed and banded them, and fit them with tiny radio collars. They then recaptured and weighed the nestlings within a few hours of fledging (at about 12 days post-hatching) to assess nestling growth rates.

sparrowbaby

Banded sparrow nestling with radio antenna trailing from below its wing. Credit: Marek C. Allen.

Three days after the birds fledged, Dudeck radio-tracked them, and surrounded them with three speakers approximately 8 meters from where they perched. For one hour, each youngster listened to recordings of calls made by predators such as ravens or hawks, followed, after a brief rest period, by one hour of calls made by non-predators such as geese or woodpeckers (or vice-versa). During the playbacks, Dudeck observed the birds to record how often the parents visited and fed their offspring, and whether offspring behavior changed in association with predator calls. This included recording all of the offspring begging calls.

BlairRadio

Blair Dudeck simultaneously uses a tracking device to locate Song Sparrows and a recorder mounted to his head to record their begging calls. Credit: Marek C. Allen.

Fear had a major impact on parental behavior. Parents reduced food provisioning vists by 37% when predator calls were played in comparison to when non-predator calls were played. They also fed offspring fewer times per visit, which resulted in 44% fewer meals in association with predator calls.

DudeckFig1

Mean number of parental provisioning visits (in one hour) in relation to whether predator (red) or non-predator (blue) calls were played. Error bars are 1 SE.

Hearing predator calls had no effect on offspring behavior – they continued to beg for food at a high rate, and did not attempt to hide.

Some parents were much more scared than others – in fact, some parents were not scared at all. The researchers measured parental fearfulness by subtracting the number of provisioning visits by parents during predator calls from the number of visits during non-predator calls. A more positive number indicated a more fearful parent (a negative number represents a parent who fed more in the presence of predator calls). The researchers discovered that more fearful parents tended to have offspring that were in poorer condition at day 6 and at fledging.

DudeckFig2

Offspring weight on day 6 (open circles) and at fledging (solid circles) in relation to parental fearfulness.  Higher positive numbers on x-axis indicate increasingly fearful parents.

Importantly, more fearful parents tended to have offspring that died at an earlier age. Based on this finding, the researchers created a statistical model that compared survival of offspring that heard predator playbacks throughout late-development with survival of offspring that heard non-predator playbacks during the same time period. They estimated a 24% reduction in survival. Combined with their previous study on playbacks during early development, the researchers estimate that hearing predator playbacks throughout early and late development would reduce offspring survival by an amazing 53%.

This “fear itself” phenomenon can extend to other trophic levels in a food web. For example recent research by Zanette and a different group of researchers showed that playbacks of large carnivore vocalizations dramatically reduced foraging by raccoons on their major prey, red rock crabs. When these carnivore playbacks were continued for a month, red rock crab populations increased sharply. This increase in crab population size was followed by a decline of the crab’s major competitor – the staghorn sculpin, and the crab’s favorite food, a Littorina periwinkle. Thus “fear itself” can cascade through the food web, affecting multiple trophic levels in important ways that ecologists are now beginning to understand.

note: the paper that describes this research is from the journal Ecology. The reference is Dudeck, B. P., Clinchy, M., Allen, M. C. and Zanette, L. Y. (2018), Fear affects parental care, which predicts juvenile survival and exacerbates the total cost of fear on demography. Ecology, 99: 127–135. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.