Carbon dioxide’s complex personality

Carbon dioxide (CO2) deservedly gets a lot of bad press because it is responsible for much of the global warming Earth is currently experiencing.  Less publicized, but perhaps equally important, CO2 is acidifying oceans, thereby threatening the continued existence of some critical biomes such as coral reefs and kelp forests (acid interferes with the ability of many marine organisms to build their shells).  But carbon dioxide also has a kinder, gentler side, as it is an essential resource for plants, and in some cases higher CO2 levels can increase a plant’s ability to carry on photosynthesis.  Sean Connell and his colleagues explored this complex personality by studying a marine ecosystem that experiences naturally varying levels of CO2. High CO2 levels and acidity exist near CO2-emitting vents at the study site – a volcanic island (Te Puia o Whakaari) off the coast of New Zealand.

White_Island_James Shook [CC BY 2.5 (https-::creativecommons.org:licenses:by:2.5)], from Wikimedia Commons

The volcanic Te Puia o Whakaari off the coast of New Zealand’s north island. Credit: James Shook [CC BY 2.5 (https-//creativecommons.org/licenses/by/2.5)], from Wikimedia Commons.

The major players in this ecosystem are the kelp, Ecklonia radiata, several species of turf-forming algae, and two grazers, the snail, Eatoniella mortoni, and the urchin, Evechinus chloroticus.  The typical vegetation in the region is a mosaic of kelp forest, some scattered small patches of algal turf, and sea urchin barrens – hard rock without significant vegetation, a result of overgrazing by sea urchins.  In contrast, extensive algal mats carpeted the rocks near these vents, and the researchers hypothesized that high CO2 levels caused this shift in dominant vegetation.

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Sean Connell collects data in a habitat dominated by algal turf (and numerous fish). Credit: anonymous backpacker.

Connell and his colleagues chose two vents and two nearby control sites at a depth of 6-8 meters. The CO2 levels and acidification near the vents were approximately equal to the amount projected for the end of the 21stcentury, but there were no differences between vents and controls in temperature, salinity or nutrient concentrations. The researchers estimated photosynthetic rates for kelp and turf algae by measuring the rate of oxygen production. They also estimated snail consumption rates by caging them for 3 days and measuring how much algal turf they removed.  They used an analogous approach to measure sea urchin consumption rates.

Conditions at vents had a major impact on both producers and consumers.  Kelp production decreased slightly, while turf production increased sharply at vents (Figures A and B below).  Urchin density declined (almost to nonexistence) while gastropod density increased markedly at vents (Figures C and D).  Lastly, consumption rates (on a per individual basis) by urchins plummeted, while consumption rates by snails increased sharply at vents (Figures E and F).

ConnellFig3

Comparison of production and consumption at control sites vs. carbon dioxide emitting vents.

These patterns converted the normal mosaic of kelp forest, small algal turf patches and urchin barren into turf-dominated habitats.  Algal turf increased in size and frequency near the vents, while kelp forest shrank into near oblivion.

ConnellFig2

Frequency of patches of turf (light gray bars), urchin barren (medium gray) and kelp (black) in relation to patch size (diameter in meters) at control sites (top graph) and sites near vents (bottom graph).

These results can be pictured visually by the graph below.  Under conditions of present-day pH and CO2 levels, gross algal production is relatively low and urchin consumption is relatively high, which results in negligible net algal turf production (net production = gross production – urchin and gastropod consumption).  High CO2 levels sharply increase gross algal turf production while dramatically decreasing consumption by urchins.  Even though gastropod consumption increases slightly at vents, the overall effect on vents is a dramatic increase of net algal turf production. Consequently, the ecosystem experiences regime shift from kelp to algal turf domination.

ConnellFig1

Summary of effects of CO2 release by vents (bottom) vs Controls (top). Net algal production (red circle) = Gross algal production – urchin and gastropod consumption.  Net algal production in dark green zone is predicted to be turf-dominated (as is found near vents), light green is a mosaic, while white zone represents urchin barrens (low production and high consumption). Error bars are 1 standard error. 

Under current conditions, kelp is the dominant producer over turf algae in the near offshore ecosystem. High consumption by urchins keep the turf algae in check.  But near CO2 emitting vents, high levels of carbon dioxide have a dual effect on this ecosystem, disproportionately increasing turf algae production rate and decreasing urchin abundance and consumption rate.  This allows the competitively subordinate turf algae to replace the competitively dominant kelp, resulting in a dramatically changed ecosystem.  This occurs in the absence of an increase in ocean temperature.  Given that ocean temperature will increase sharply by 2100 (along with CO2 levels), many species interactions are expected to change in the next century, and ecosystem structure and functioning will be very different from what we observe today.

note: the paper that describes this research is from the journal Ecology. The reference is Connell, S. D., Doubleday, Z. A., Foster, N. R., Hamlyn, S. B., Harley, C. D., Helmuth, B. , Kelaher, B. P., Nagelkerken, I. , Rodgers, K. L., Sarà, G. and Russell, B. D. (2018), The duality of ocean acidification as a resource and a stressor. Ecology, 99: 1005-1010. doi:10.1002/ecy.2209 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.

Recruiting rhinoceros

Despite their immense size and unfriendly disposition, we humans have done an excellent job decimating the black rhinoceros (Diceros bicornis) population from several hundred thousand individuals around 1900 to fewer than 3000 individuals by 1990. Three subspecies are extinct, one is on the brink, while even the most successful remaining subspecies, the south-central black rhinoceros, is extinct over much of its former range, or only found in nature reserves.  Humans prize its horns, which historically were used for making wine cups, ceremonial daggers, and a variety of medicines that purportedly revive comatose patients, detoxify infections, and aid male sexual stamina. Trade of rhinoceros horn has been illegal since 1977, but poaching abounds.

rhinohornprodblog

Rhinoceros horn products seized by the Hong Kong Government. Credit: U.S. Government Accountability Office from Washington, DC, United States [Public domain], via Wikimedia Commons

This population crisis has motivated conservation ecologists to evaluate the best approaches to conserving the black rhinoceros, and to restoring it to parts of its former range. Translocation, moving rhinoceroses from one location where they are relatively well-established, to another where they are extinct or at very low numbers, is a viable approach to restoring populations. However, translocation did not always work well, as some rhinoceroses died following translocation, or failed to reproduce even if they survived translocation. While a post-doctoral researcher at the Zoological Society in San Diego, California, Wayne Linklater recognized that there were large datasets collected by government and non-government agencies that might answer the question about what drives better rhinoceros survival and breeding.  Unfortunately some of these datasets were difficult to access or interpret, but Jay Gedir, Linklater and several other colleagues persevered and combed through the data to identify the factors associated with successful translocation.

Dales photos Oct04 006

Black rhino is airlifted to temporary captivity before being translocated to a release site. Credit: Andrew Stringer

Many translocation studies use a short-term measure of success, such as survival or fecundity (fertility) of the translocated individuals.  The researchers reasoned that the most important measure, when it is available, is the number of offspring produced by translocated females that survive to an age that they too can reproduce, which in the case of rhinoceros is four years. Based on existing long-term studies, Gedir, Linklater and their colleagues compiled the offspring recruitment rate (ORR), which combines the variables of survival, fecundity, and offspring survival to sexual maturity. They found that ORR was greatest when mature females were translocated into a population that had a female-biased sex ratio.

conbiofig1

Offspring recruitment rate (per year) in relation to age at release and sex ratio bias of the recipient population. Female bias is greater than 60% female, male bias is greater than 60% male. Numbers above graph are sample size for each category. Error bars are 95% confidence intervals.

So why does sex-ratio matter?  The researchers are not certain, but females are subjected to considerable sexual harassment by very aggressive males, so a female-biased sex ratio may lead to less harassment and improved survival and reproductive success for translocated females.

Translocated juveniles took longer to produce their first calf after reaching sexual maturity than did adults after being released. Again this effect was stronger with a male-biased sex ratio.

conbiofig2a

Mean time (years) to produce their first calf after reaching sexual maturity for juveniles, or after release for adults.

Many females (47%) produced no surviving offspring. This pattern of recruitment failure was most common in juveniles, and least common in adults translocated into populations with a female-biased sex ratio.

conbiofig2b

Recruitment failure of translocated females in relation to age at release and sex ratio bias of the recipient population.

Several factors can cause recruitment failure: 23% of females died following translocation and 24% of surviving females never produced calves. However, calf survival to sexual maturity was a robust 89%, and this survival rate was independent of age at translocation or population sex ratio. Among surviving translocated females, juveniles were about twice as likely as young or old adults to fail to produce a calf, but were equally successful at raising the calves they were able to produce.

Linklater was surprised at how important sex ratios (and presumably social relationships) were, particularly given that black rhinoceroses spend much of their time alone or with one offspring.

Neto and Gwala size each other up

Neto (the ranger) and Gwala (the rhino) size each other up.  Credit: Wayne Linklater.

The study did not support a major role for many other factors that had previously been considered important in translocation success, such as habitat quality, population density, number of rhinoceroses released and reserve size. Based on their analysis, the researchers recommend that conservation biologists should translocate mature females into populations with female-biased sex ratios to reduce rates of recruitment failure.  If juveniles must be translocated, they too should be moved into populations that already have a female-biased sex ratio to reduce levels of sexual harassment by males after they mature.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Gedir, J. V., Law, P. R., du Preez, P., & Linklater, W. L. (2018). Effects of age and sex ratios on offspring recruitment rates in translocated black rhinoceros. Conservation Biology32(3), 628-637. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. 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.

MartinezFig1

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.

MartinexFig3

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.

 

A tale of too many ticks

Many people I know have had the unfortunate experience of a warm season bout with the following symptoms: fatigue, achy joints, headaches, dizziness, fever and night sweats. Some of these symptoms are part of the daily experience of someone who has reached my level of maturity (okay – age), but in combination they suggest infection by the bacterium Borrelia burgdorferi that is transmitted by Ixodes ticks, and causes Lyme disease.  So three years ago, when I experienced those symptoms, I went off to my doctor (after some prodding by my wife) who immediately prescribed a regime of antibiotics that is effective against Lyme. My region of the United States (southern Appalachians) is a center of Lyme infection, so the diagnosis was pretty easy, and thankfully, the antibiotics were effective.

Lyme 2016

Each dot represents one verified case of Lyme disease in the United States in 2016.  I live in the dark blotch in western Virginia.

Richard Ostfeld began investigating the ecology of Lyme disease as a result of a chance event.  About 26 years ago Ostfeld started a new project that explored how white-footed mice may control populations of the invasive forest pest, the gypsy moth.  Mice eat the moth pupae for a couple of weeks in mid-summer.  When he started trapping at the Cary Institute of Ecosystem Studies in New York, he was amazed to see tremendous burdens of larval blacklegged ticks attached to the white-footed mouse (Peromyscus leucopus).  At the field site there was a boom one year and a crash the following year in acorn abundance, which was followed, with a one year time lag, by a boom and a crash in mouse abundance.  Ostfeld wondered what role fluctuating mouse abundance might play in human risk of exposure to tick-borne disease, and how factors affecting mouse abundance might influence the system.

Mouse with 52 larval ticks closeup

This unfortunate mouse harbors 52 larval ticks. Credit: Ostfeld lab at Cary Institute.

Ixodes ticks have a two-year lifecycle, with eggs laid in the spring, six-legged larvae hatching out in summer, getting one blood meal from a rodent or bird host, and emerging as eight-legged nymphs the following spring.  Nymphs find themselves a second host in spring or summer, from which they suck more blood and ultimately metamorphose into adults during the fall season. Adults seek large mammalian hosts, such as white-tailed deer; females feed on the deer, mate with males (who generally don’t feed), lay eggs and die, usually the following spring.

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Human finger with (left to right) adult female, adult male, nymph and larval ticks. Credit: Ostfeld lab at Cary Institute.

What makes these ticks tick? Ostfeld, Taal Levi and their colleagues knew from previous work that biotic factors such as mice, acorns and deer were likely to be important, but that predators on mice might also play a role.  It also seemed likely that abiotic factors such as temperature, moisture and snow cover could also be important.  For 19 years, the researchers systematically collected data related to these factors from six large (2.25 ha) field plots at the Cary Institute. They used standard capture-mark-recapture methods to estimate rodent abundance, and data from the Cary Institute’s bow-hunting program to estimate deer abundance. They monitored the presence of carnivores with LED camera traps that were baited with cans of cat food.

coyote-camera-trap.jpg

Coyote captured on LED camera. Credit: Ostfeld lab at Cary Institute.

Lastly, the researchers needed to estimate tick abundance and the percentage of ticks that were infected with the Lyme disease bacterium, Borrelia burgdorferi.  To estimate tick abundance, the researchers systematically dragged 1-m2 white corduroy drag cloths across each plot every three weeks throughout the times of peak tick abundance. Ticks that are searching for a host (known as questing ticks) will grab onto the drag cloth, so in essence, drag cloth censuses provides an estimate of ticks that have not had a blood meal.  Tick infection rates were estimated by subjecting an average of 378 ticks per year to molecular analyses (initially direct immunofluorescence assay, and later quantitative PCR).

tick

Researchers sample for questing ticks by dragging a cloth across the forest floor. Credit: Ostfeld lab at Cary Institute.

Across the 19 years of the study, the density of infected nymphs was strongly correlated to mouse density the previous year, and weakly correlated with deer density two years previously.  Recall the details of the two-year life cycle; it takes a year to go from tick larva to nymph, and a second year to go from nymph to adult to eggs, so these time lags are not surprising. What is surprising is that the density of infected nymphs is negatively correlated with mouse density in the current year and with winter warmth.

OstfeldFig2

Density of infected ticks (x 100) per 100 m2 in relation to (far left) mouse density (per 2.25 ha) in the previous year, (2nd from left) mouse density in the current year, (2nd from right) winter warmth, and (far right) deer density two years previous.  Different color dots represent the six different field sites.

Ostfeld and his colleagues explain that during years of high mouse abundance, many nymphs were attached to rodent hosts, or had already had a blood meal, and thus were not collected on drag cloths. By using the abundant rodents as their secondary hosts, rather than people, high rodent abundance is actually decreasing the probability that the nymphs will infect a human. Infection of humans by adult ticks is less common than infection of humans by nymphs, because many nymphs don’t survive to adulthood, male adults do not feed, and adults are more likely than nymphs to be spotted and removed, due to their larger size.

Nymphal infection prevalence (NIP) measures the fraction or proportion of the nymphs within the community that are actually carrying the bacterium.  From a human perspective, a high NIP indicates that a tick bite is relatively likely to lead to Lyme disease. There was only a small relationship between rodent density the previous year and NIP, so the researchers decided to see if the composition of the predator community might influence NIP. They reasoned that foxes and bobcats were known to be major mouse predators, so by eating mice, they would be removing infected ticks from the population.  Raccoons and opossums have a double effect; they eat mice – though not as many as do foxes and bobcats.  In addition they are dilution hosts, in that they provide blood for nymphs, but do not serve as a vector to the bacterium.  Thus a community with all four of these predators was expected to reduce NIP. The effect of coyotes were more complex because they eat mice, which should reduce NIP, but they also eat or scare away other predators, such as foxes and opossums, which could increase NIP.

OstfeldFig4

Effect size of predator community structure on nymphal infection prevalence (NIP).  Top row animals are (left to right) fox, raccoon, opossum and bobcat.  Communities with coyotes (bottom five communities) tend to have higher NIP, particularly if they lack other predators.

In general, more diverse predator communities tended to have lower nymphal infection prevalence.  Communities with coyotes that also lacked some of the other predators tended to have the highest NIP values.

Ostfeld and his colleagues were surprised to discover that a warm and dry winter and spring season tended to depress tick abundance, while cold winters had little effect. Presumably, emerging nymphs can dry out under warm, dry conditions. The researchers were also surprised to observe the strong decrease in tick abundance associated with high mouse abundance in the current year. It is not uncommon for a boom in mouse abundance one year to be followed by a mouse population crash the next year.  When that occurs, there will be a large number of questing nymphs lurking in the vegetation for hosts, and thus the potential for a major outbreak of Lyme disease.

note: the paper that describes this research is from the journal Ecology. The reference is Ostfeld, R. S., Levi, T. , Keesing, F. , Oggenfuss, K. and Canham, C. D. (2018), Tick‐borne disease risk in a forest food web. Ecology, 99: 1562-1573. doi:10.1002/ecy.2386. 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.

Finding fish fluorescently

Very early in my teaching career at Carleton College in Minnesota, I was thrust into the position of teaching students about things that I knew very little about.  I quickly learned that things went well, so long as I confessed my ignorance – the very bright students at that college were always happy to help me with my education. My ignorance of things biological stemmed from my undergraduate training in psychology, which had only a smattering of biology and chemistry in the coursework.  So when we extracted chlorophyll from a plant, shone a bright high-energy (probably UV) light on it, and it glowed a beautiful red, my reaction was “wooo…, that’s cool.”  My colleague, who was much more broadly trained, explained that this process, biofluorescence, occurred because the chlorophyll’s electrons were excited by the high energy light, and that they emitted the red light when they returned to a lower-energy state.

Marteenfig1Solenostomus cyanopterus

Robust ghost pipefish, Solenostomus cyanopterus, is cryptic in ambient daylight (left), but biofluoresces red when lit at night by a high-intensity LED torch (right).

 

Many threatened or endangered marine species are cryptic, providing challenges to conservation biologists who must assess the abundance of these species.  Usually, marine biologists use underwater visual censuses to measure abundance and distribution of marine species, but small or cryptic species are often missed or undercounted.  Maarten de Brauwer reasoned that conservation biologists could use biofluorescence as a tool to find small or cryptic marine organisms.  He knew from a paper that recently came out in the literature, and from his own experience as a diver, that a number of cryptic species do fluoresce. But how large is that number?

marteenfig2

A diver searches for biofluorescent species. Credit: J. A. Hobbs

DeBrauer, working with five other researchers, surveyed reef fish at four locations in Indonesia, as well as two locations outside Indonesia (Christmas Island and the Cocos Islands).  Indonesia was a conservation priority as it contains the world’s greatest abundance of marine fish species. Using high-energy LED torches, the researchers surveyed 31 sites at the six locations, assessing each fish they detected for whether it was cryptic or non-cryptic, and whether it fluoresced. Of 95 cryptic species, 83 fluoresced.  In contrast, only 12 of 135 non-cryptic species fluoresced.

MarteenEcolFig1

Number of cryptic and non-cryptic species showing biofluorescence in the survey.

Why are cryptic species more likely to biofluoresce?  As it turns out, we don’t know the answer to this question.  De Brauwer suggests that some small species, like gobies and triplefins, may use flourescence, which is particularly well-defined around the head region, as a way of communicating without predator detection.  These species fluoresce in red, a very-short-range light, so predators won’t see them unless they are very close. Some species of scorpionfish that live in algae and seagrass also fluoresce red, which allows them to blend in well with the red fluorescence emitted by the algal and seagrass chlorophyll.

Having shown that cryptic species tend to bioflouresce, the next challenge was to see whether bioflourescence surveys worked better than standard underwater visual censuses. First, the researchers focused their efforts on two species of pygmy seahorses (Hippocanpus bargibanti and H. denise) that live on seafans, searching for two minutes, either with or without a flourescence torch.  They followed with a similar study on two species of reef fish, the largemouth triplefin (Ucla xenogrammus) and the highfin triplefin (Enneapterygius tutuilae); but this time surveying 20m x 2m transects, either with or without a fluorescence torch.

marteenfig3.jpg

A diver searches a seafan for pygmy seahorses. Credit: J. A. Hobbs.

Unfortunately, the pygmy seahorses are tiny (as you might suspect from their name) and probably rare, so only 32 H. bargibanti and 7 H. denise were detected. These seahorses fluoresce red primarily in their tail region and green from their eyes.

MarteenEcolFig3

Two cryptic pygmy seahorses “seen” under ambient light (left, circled in red) and in the underwater biofluorescence census (right).

The numbers of H. denise were too small to include in the analysis. But for the other three species, the bioflourescence surveys detected more individuals than did the underwater visual surveys.

MarteenEcolFig4

Mean number of individual H. bargibanti (left), U. xenogrammus (center) and E. tutuilae (right) detected with underwater visual surveys (UVC) vs. underwater biofluorescence surveys (UBC).

The researchers discovered that bioflourescence is very common in these cryptic and rare species, which means this technique can be used to assess abundance in species most likely to be overlooked using standard underwater visual surveys. The International Union for the Conservation of Nature, which (among other tasks) is responsible for assessing the extinction risk of species worldwide, has only been able to do so for less than 44% of fish belonging to three large cryptic families of reef fish.  Of 2000 species in these three families, 21% are listed as data-deficient because they have been so difficult to survey.  This novel approach should help inform conservation biologists about species that are in dire straits, so they can focus conservation efforts in a productive and useful direction.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Brauwer, M., Hobbs, J. A., Ambo‐Rappe, R., Jompa, J., Harvey, E. S. and McIlwain, J. L. (2018), Biofluorescence as a survey tool for cryptic marine species. Conservation Biology, 32: 706-715. doi:10.1111/cobi.13033. You should also check out Dr. De Brauwer’s blog at crittersresearch.com. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.

Seaweed defense – location, location, location.

If you’re ever feeling sorry for yourself, you should know that things could have been much worse; you could have been the brown seaweed, Silvetia compressa. So many problems!  Ocean waves come crashing over you, threatening to pull you off your life-sustaining substrate.  Ocean tides recede, exposing you to harsh sun and dangerously dry conditions. Perhaps worst of all, the fearsome predator Tegula funebralis eats away at your body, and you are powerless to defend yourself from its savage ravages.

MoatCreek_SilvetiaTegula

Tegula snails chomp away on Silvetia seaweed in northern California. Credit: Emily Jones.

As it turns out, Silvetia is not so powerless after all.  After being partially grazed by Tegula, the seaweed can induce defenses that reduce its palatability.  From prior work, Emily Jones noticed that seaweed from northern California shorelines was much more sensitive to grazing than was seaweed from southern California shorelines.  It took fewer grazing snails to elicit palatability reduction in northern Silvetia than it did in southern Silvetia. She decided to focus her PhD work with Jeremy Long on documenting these geographic differences, and figuring out why they exist.

MoatCreek_surveys

Emily Matthews (near) and Grace Ha (far) survey snails and seaweed in a northern California site. Credit: Emily Jones.

Environmental conditions vary along the California coast.  Northern seaweed populations experience cooler temperatures (air ~5-20 °C; water ~10-12 °C) and more nutrients (nitrate levels up to 40 umol/L) than do southern populations (air 5-37 °C; water ~14-20 °C; nitrate levels < 2 umol/L). In addition, Jones and Long surveyed Tegula abundance at three northern California and three southern California sites, counting every snail in 20 quadrats placed in the low, mid and high intertidal zone at each of the six sites (360 0.25 X 0.25m quadrats in total) .  They discovered that seaweed was much more likely to encounter Tegula along northern coastlines.

JonesFig1

Percent of plots with Tegula snails in northern sites (Stornetta, Moat Creek and Sea Ranch – blue bars) and southern sites (Coast, Calumet and Cabrillo – orange bars). High, Mid and Low refer to location within the intertidal zone (high is closest to shore and regularly exposed at low tide).

Given these differences in snail abundance, we can now understand why Silvetia is more sensitive in its northern range to Tegula grazing.  But how strong are these differences in sensitivity? Jones and Long developed a simple paired-choice feeding preference assay to test for differences in palatability. At each location (north and south), the researchers gave test snails a choice between feeding on seaweed that had been previously grazed by either 1, 4, 7, 10 or 13 Tegula snails, or to feed on seaweed with no grazing history.  The test snails grazed for five days, and the researchers measured the amount of seaweed consumed for each group. They discovered that even a little bit of previous grazing (the 1-snail treatment) made northern test snails prefer non-grazed northern Silvetia, while only high levels of previous grazing (the 10 and 13-snail treatments) had similar effects on southern snails tested on southern Silvetia.

JonesFig2

Amount of previously-grazed and non-grazed Silvetia eaten by Tegula in paired choice tests. (Top) Northern Selvetia, (Bottom) Southern Silvetia. Error bars are 1SE. * indicates significant differences in consumption rate.

These findings raised the question of whether the cooler and more nutrient-rich environmental conditions at the northern site were somehow causing this difference in consumption of previously-grazed seaweed.  The researchers designed a series of common garden experiments at the Bodega Marine Laboratory, in which seaweed from both locations were tested in the same environment.  Silvetia was exposed to grazing by two snails, or by no snails for 14 days. When test snails were given the choice of non-grazed or previously-grazed northern Silvetia, they much preferred eating non-grazed Silvetia. In contrast, they showed no preference when given a similar choice between non-grazed or previously-grazed southern Silvetia. This indicates that seaweed from the north are responding more to grazing by reducing palatability than are seaweed from the southern locations.

JonesFig5

Amount of previously-grazed and non-grazed northern and southern Silvetia eaten by Tegula in paired choice tests.

In theory, there could be a tradeoff between induced defenses, such as reduction in palatability in response to grazing, and constitutive defenses, which an organism expresses all of the time.  Examples of constitutive defenses are thorns or spines in plants, and cryptic coloration or body shape in many insects.  Jones and Long found no evidence for such a tradeoff; in contrast southern Silvetia actually had lower levels of constitutive defenses, as both northern and southern Tegula strongly preferred eating southern Silvetia in paired choice tests.

JonesFig6

Amount of northern and southern Silvetia eaten by northern and southern Tegula in paired choice tests.

These geographic differences in seaweed sensitivity to grazing are probably due to long-term differences in environmental history.  Southern Silvetia seaweeds live in stressful conditions (high temperatures and low nutrients), and the physiological cost of mounting an induced defense against low and moderate levels of grazing may be too high to be worthwhile. We also don’t know what the overall grazing rates are in the north versus the south, and importantly, how variable the grazing rates are in each location.  Highly variable grazing rates would select for a strong set of induced responses, which could be turned on and off as needed, allowing seaweed, or any plant, to defend itself against new or more hungry herbivores moving into their environment.

note: the paper that describes this research is from the journal Ecology. The reference is Jones, Emily and Long, Jeremy D. 2018. Geographic variation in the sensitivity of an herbivore-induced seaweed defense. Ecology. doi: 10.1002/ecy.2407. 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.

Indirect effects of the lionfish invasion

I’m old enough to remember when ecological studies of invasive species were uncommon.  Early on, there was a debate within the ecological community whether they should be called “invasive” (which conveyed to some people an aggressive image akin to a military invasion) or more dispassionately “exotic” or “introduced.” Lionfish (Pterois volitans), however, fit this more aggressive moniker. Native to the south Pacific and Indian Oceans, lionfish were first sighted in south Florida in 1985, and became established along the east Atlantic coast and Caribbean Islands by the early 2000s. They are active and voracious predators, consuming over 50 different species of prey in their newly-adopted habitat. Many population ecologists study the direct consumptive effects of invasive species such as lionfish.  In some cases they find that an invasive species may deplete its prey population to very low levels, and even drive it to extinction.

Lionfish

A lionfish swims in a reef. Credit: Tye Kindinger

But things are not always that simple. Tye Kindinger realized that lionfish (or any predator that feeds on more than one species) could influence prey populations in several different ways.  For the present study, Kindinger considered two different prey species – the fairy basslet (Gramma loreto) and the blackcap basslet (Gramma melacara). Both species feed primarily on zooplankton, with larger individuals monopolizing prime feeding locations at the front of reef ledges, while smaller individuals are forced to feed at the back of ledges where plankton are less abundant, and predators are more common.  Thus there is intense competition both within and between these two species for food and habitat. Kindinger reasoned that if lionfish depleted one of these competing species more than the other, they could be indirectly benefiting the second species by releasing it from competition.

Basslets

Fairy basslet (top) and blackcap basslet (bottom). Credit Tye Kindinger.

For her PhD research, Kindinger set up an experiment in which she manipulated both lionfish abundance and the abundance of each basslet species.  She created high density and low density lionfish reefs by capturing most of the lionfish from one reef and transferring them to another (a total of three reefs of each density).  She manipulated basslet density on each reef by removing either fairy or blackcap basslets from an isolated reef ledge within a particular reef.  This experimental design allowed her to separate out the effects of predation by lionfish from the effects of competition between the two basslet species.  Most of her results pertained to juveniles, which were about 2 cm long and favored by the lionfish.

KindingerTable

Alex Davis

Alex Davis captures and removes basslets beneath a ledge. Credit Tye Kindinger.

Kindinger measured basslet abundance in grams of basslet biomass per m2 of ledge area.  When lionfish were abundant, juvenile fairy basslet abundance decreased over the eight weeks of the experiment (dashed line) but did not change when lionfish were rare (solid line).  In contrast, juvenile blackcap basslet populations remained steady over the course of the study, whether lionfish were abundant or rare. Kindinger concluded that lionfish were eating more fairy basslets.

KindingerFig12A

Abundance of juvenile fairy basslets (left) and blackcap basslets (right) as measured as change in overall biomass. Triangles represent high lionfish reefs and circles are low lionfish reefs.

Competition is intense between the two basslet species, and can affect feeding position and growth rate.  Kindinger’s manipulations of lionfish density and basslet density demonstrate that fairy basslet foraging and growth depend primarily on the abundance of their blackcap competitors. When competitor blackcap basslets are common (approach a biomass value of 1.0 on the x-axis on the two graphs below), fairy basslets tend to move towards the back of the ledge, and grow more slowly.  This occurs at both high and low lionfish densities.

KindingerFig1BC

Change in feeding position (top) and growth rate (bottom) of fairy basslets in relation to competitor (blackcap basslet) abundance (x-axis) and lionfish abundance (triangles = high, circles = low)

In contrast, blackcap basslets had an interactive response to fairy basslet and lionfish abundance. Let’s look first at low lionfish densities (circles in the graphs below).  You can see that blackcap basslets tend to move towards the back of the ledge (poor feeding position) at high competitor (fairy basslet) biomass, and also grow very slowly.  But when lionfish are common (triangles in the graphs below), blackcap basslets retain a favorable feeding position and grow quickly, even at high fairy basslet abundance.

KindingerFig2BC

Change in feeding position (top) and growth rate (bottom) of blackcap basslets in relation to competitor (fairy basslet) abundance (x-axis) and lionfish abundance (triangles = high, circles = low)

By preying primarily on fairy basslets, lionfish are changing the dynamics of competition between the two species. The diagram below nicely summarizes the process.  Larger fish of both species forage near the front of the ledge, while smaller fish forage further back.  But there is an even distribution of both species.  Focusing on juveniles, they are relatively evenly distributed in the rear portion of the ledge (Figure B).  When fairy basslets are removed experimentally, the juvenile blackcap basslets move to the front of the rear portion of the ledge, as they are released from competition with fairy basslets (Figure D).  Finally, when lionfish are abundant, fairy basslets are eaten more frequently, and juvenile blackcaps benefit from the lack of competition (Figure F)

KindingerFig3

Kindinger was very surprised with the results of this study because she knew the lionfish were generalist predators that eat both basslet species, so she expected lionfish to have similar effects on both prey species.  But they didn’t, and she does not know why.  Do lionfish prefer to eat fairy basslets due to increased conspicuousness or higher activity levels, or are blackcap basslets better at escaping lionfish predators? Whatever the mechanism, this study highlights that indirect effects of predation by invasive species can influence prey populations in unexpected ways.

note: the paper that describes this research is from the journal Ecology. The reference is Kindinger, T. L. (2018). Invasive predator tips the balance of symmetrical competition between native coral‐reef fishes. Ecology99(4), 792-800. 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.