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.

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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.

Kelp consumption curtailed by señorita

Miranda Haggerty was diving through a kelp forest, and noticed that many kelp bore a large number of tiny limpets that were housed in small scars that they (or a fellow-limpet) had excavated on the kelp’s surface. This got her thinking about how these scars might affect the kelp, and equally relevant, whether there were any limpet predators that might lend the kelp a hand (or a mouth) by removing limpets.

Jerry Kirkhart

A limpet grazes on a kelp frond. Credit: Jerry Kirkhart

Feather boa kelp (Egregia menziesii) is a foundation species within the subtidal marine system off the California coast, providing food and habitat for many species that live on or among its fronds. The tiny seaweed limpet, Lottia insessa, specializes on feather boa kelp, grazing on its fronds and living within the scars. Many invertebrates and fish live within the kelp forest, but the most abundant fish is the señorita, Oxyjulis californica. Haggerty wondered whether the señorita might benefit the kelp (directly) by removing limpets, or (indirectly) by scaring limpets away – what ecologists call a trait-mediated indirect interaction.

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The señorita – a fearsome predator of limpets.  Credit: Miranda Haggerty

The first order of business was to determine whether the limpets were actually harming the kelp.  Haggerty and her colleagues approached this in two ways.  First they chose 94 kelp plants from kelp forests off the California coast.  From each individual they chose one grazed and one ungrazed frond (each 3 m long). Grazed fronds averaged 5-10 scars and at least 2 limpets per meter of length.  Every three weeks they visited their kelp to score for broken fronds. In 29 of 30 cases, the grazed frond broke before the ungrazed frond (in the remaining cases the entire plant was missing, or both fronds broke and the researchers could not tell which had broken first).

HaggertyFigS1

Photo of feather boa kelp showing grazing scars, including one housing a limpet (left).  Diagram of feather boa kelp showing multiple fronds (right).

But the researchers were concerned that perhaps limpets chose to graze on weaker fronds, so the breakage was not caused by grazing scars, but by limpet choice.  To account for this concern, Haggerty and her colleagues chose 43 ungrazed kelp plants, placed three  limpets on one frond, and chose a second, equal-sized frond as an unmanipulated control. Once again, they visited their plants every three weeks, and discovered that grazed fronds broke first in all 20 pairs that the sequence of frond breakage could be determined.  Clearly, limpet grazing is bad news for feather boa kelp.

How does the señorita fit into this system? The researchers designed a laboratory experiment to address this question.  They used 10 large tanks (1700 L), and set up five different experimental treatments to compare direct effects of predation, and indirect effects of predator presence, on limpet grazing, and ultimately on kelp survival. To isolate the direct effects of predation from the indirect effects of predator cues on limpets, Haggerty and her colleagues placed four kelp fronds into fish exclosure cages, which were housed in the large tanks, and placed three limpets onto some of these fronds.  To mimic actual predation (CE treatment in Table below), they removed limpets by hand at a constant rate typical of señorita predation. For the NCE treatment (testing indirect effects of predator presence) they introduced señorita into the large tank so the limpets experienced the predator cues, but were not eaten. The different treatments are summarized in the table below. These experiments ran for one week and each treatment was replicated 10 times.

HaggertyTableFinalEach day the researchers monitored the number of limpets and grazing scars.  After one week, Haggerty and her colleagues counted the number of grazing scars, and measured the breaking strength of each frond by clamping the frond’s end to a table and pulling on the opposite end with a spring scale until it broke. They then recorded the amount of force needed to break the frond.

brokenkelp.jpg

Clamped kelp frond whose breaking strength has been tested.  Notice that the frond broke at a grazing scar (right). Credit Miranda Haggerty.

Not surprisingly, the predator control (PC) kelp (limpets present without señorita) had the most scars and lost the greatest amount of tissue.  Kelp receiving the consumptive predator effect treatment (CE) had fewer scars and lost less tissue than PC.  But interestingly, kelp receiving NCE and TPE treatments had significantly fewer scars than the CE kelp, and were statistically indistinguishable from each other.  Thus, in the laboratory, the presence of señorita cues (NCE treatment) was more important than actual predation (CE treatment) in reducing kelp scarring and tissue consumption (top and middle graph below).  As a result, the NCE treated kelp were stronger (had greater breaking strength) than were the CE treated kelp (bottom graph below).

HaggertyFig2

Mean (+ standard error) number of grazing scars (top), mass of tissue consumed (middle) and breaking strength (bottom) of kelp in response to five experimental treatments. CE = consumptive effect, NCE = non-consumptive effect, TPE = total predator effect, PC = predator control, LC = limpet control. Different letters above bars indicate significant differences between the means when comparing treatments.

Haggerty and her colleagues replicated this experiment, with a few experimental design modifications, in a field setting.  As with the laboratory experiment we’ve just discussed, the researchers found a very strong non-consumptive effect. The researchers suspect that these limpets respond to chemical cues emitted by their señorita predators. They could not respond to many types of sensory cues because they lack auditory organs, and the experimental design prevented fish from transmitting any shadows (visual cues) or vibrational cues. In addition previous studies have shown that some limpet species use chemoreception for predator avoidance, foraging and homing. However, the nature of this chemical cue is yet to be discovered for this predator-prey system.

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Schooling señorita. Credit: Miranda Haggerty

Trophic cascades occur when the effects of one species on another species cascade down through the ecosystem. In this case, señorita predators directly and indirectly reduce limpet density, which increases the survival of kelp – a foundation species for this ecosystem. The researchers point out that this trophic cascade only occurs in the southern feather boa kelp range, because señorita are absent further north.  We don’t know if limpets have other predators in the northern range, but we do know that the kelp are structurally more robust further north, so they (and the ecosystem) may be relatively immune to limpet-induced destruction.

note: the paper that describes this research is from the journal Ecology. The reference is Haggerty, M. B., Anderson, T. W. and Long, J. D. (2018), Fish predators reduce kelp frond loss via a trait‐mediated trophic cascade. Ecology, 99: 1574-1583. doi:10.1002/ecy.2380. 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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.