Purple Sea Urchins: Survivors in an Acidic Ocean?

Purple sea urchins residing in small hollows excavated in a reef. Photo copyright Anne M. Rosenthal.

What happens to ocean animals as increasing carbon dioxide acidifies the ocean? Can populations evolve quickly enough to survive?

Along the Pacific Coast, that just might happen: Intermittent upwelling from the deep already brings marine organisms into contact with acidic waters. And to survive, populations must harbor gene versions – alleles – that allow them to cope with an acidic pH. But how rapidly can these adaptive alleles become dominant in a population? Experiments by Melissa H. Pespeni and colleagues, in the Palumbi laboratory at Hopkins Marine Station, Stanford University, showed surprisingly fast adaptation in larval populations of the purple sea urchin, Strongolocentrotus purpuratus.

A fragment of the test or skeleton of the purple sea urchin. The tiny holes are pores where tube feet protrude through the test. Photo copyright Anne M. Rosenthal.

One of the most strikingly beautiful invertebrates along West Coast seashores, S. purpuratus sports the  calcareous skeleton typical of sea urchins, a "test" complete with moveable spines, as well as pores where tube feet – sucker-tipped extensions of its hydraulically operated water vascular system – protrude. Like sea stars, brittle stars, and sea cucumbers, sea urchins are members of the phylum Echinodermata and bear both bilateral and radial symmetry. 

As vegetarians, purple sea urchins consume a variety of algae, gnawing away with five renewable teeth, part of a mouth complex known as Aristotle's lantern. The purple sea urchin's teeth, and most likely its spines, also come in handy for excavating urchin apartment complexes – clusters of urchin-sized hollows located in reefs where conditions are optimal for urchin survival. Urchins serve as prey for their close cousins, the sea stars, and are favored morsels for sea otters, apex predators that keep urchin populations under control; urchin pigment even collects in the bones of otters, staining them purple.

The magnificent purple sea urchin bears rows of spines in a radial symmetry. Photo copyright Anne M. Rosenthal.

Sea urchin life begins when females and males release millions of eggs and sperm into the ocean, a process known as broadcast spawning. When sperm meets egg, fertilization occurs, and the egg begins to divide, forming a swimming pluteus larva within two to four days. For a fascinating video of urchin egg division and pluteus larvae, see the Plankton Chronicles YouTube channel: http://www.planktonchronicles.org/en/episode/sea-urchin-planktonic-origins

Skeletal rods composed of calcite (CaCO3) are instrumental to the larva's ability to swim and feed, and thus, to its survival over four or so months of drifting and feeding within the plankton before settling down to become a sessile adult.

Micrograph of the pluteus larva of a sea biscuit, a type of sand dollar, showing the skeletal rods. Photographed under polarized light microscopy by Bruno C. Vellutini.

But here's the bottom line for an urchin larva: It has to extract calcium carbonate from ocean water to build its skeletal rods more quickly than they dissolve back into the ocean. And the more acidic the water, the faster calcium carbonate dissolves.

Sea urchin larva. Photo courtesy of Stephen Palumbi.

Carbon dioxide comes into play because, when it is absorbed by water, it forms carbonic acid. Therefore, as carbon dioxide concentrations increase in the air, ocean waters gradually acidify. This process is spelled out in a viewer-friendly video by Stephen Palumbi, Stanford University (Hopkins Marine Station) on the Microdocs YouTube channel: http://tinyurl.com/17fvbs3

Compared to other organisms, purple sea urchins have a head start in terms of genetic diversity. One study showed that purple sea urchin populations bear more versions of their genes than any other organism yet studied – approximately a thousand times more than humans, for example. But would this genetic diversity confer survival of some individuals under acidic conditions predicted for the future? And if so, would an actual shift in the frequency of adaptive alleles be observed under conditions of lower pH?

Prior experiments with S. purpuratus grown in the laboratory had shown poor larval survival in water acidified to the future levels anticipated. However, judging that crowded conditions and still waters might have stymied survival in previous experiments,  Pespeni and colleagues designed a new experiment featuring more spacious quarters and continuous water movement akin to the constantly shifting ocean.

Melissa Perpeni injects urchin to prompt spawning. Photo by Dan Griffin, courtesy of Stephen Palumbi.

Spawning sea urchins in laboratory. Photo by Dan Griffin, courtesy of Stephen Palumbi.

Male and female sea urchins were then collected from seven populations along 1200 kilometers of the Pacific Coast. For each population, scientists mixed eggs from ten females with a mixture of sperm from ten males. Resulting planktonic larvae were raised under today's ambient CO2 conditions or under experimentally elevated CO2 representative of likely future conditions.

Melissa Pespeni uses a microscope to check on sea urchin larvae. Photo by Dan Griffin, courtesy of Stephen Palumbi.

Then, using advanced molecular biology techniques, Pespeni monitored the collective genome of both populations of sea urchin larvae – those under present-day pH and those under anticipated acidic conditions – over time as the larvae matured. Despite few telltale differences in size or appearance, rate of development, or competency to settle, there were pronounced genetic changes in the population of surviving experimental larvae as time went on. These genetic changes were, in fact, related to cellular processes that regulate pH and build skeletons.

The findings indicated the beginning of an evolutionary response to increased acidity and implied that purple sea urchin populations not only have the genetic components to survive lower pH levels, but that the level of these alleles can quickly increase in purple sea urchin populations.

Yet this might or might not benefit the population in the long run, notes Pespeni on her web site, since concurrent loss of genetic diversity could cost the sea urchin population in other ways. Specifically, as a result of evolving to survive acidic conditions, the population might no longer have sufficient plasticity to respond successfully to other environmental pressures, such changes in temperature, fluctuations in food availability, or presence of disease-causing organisms. Further research may lend insight to whether sea urchin populations can adapt to multiple stressors simultaneously.

But an even bigger question looms on the horizon, indicates Pespini. While genetic resilience to ocean acidification in purple sea urchin populations looks promising, what about organisms with tiny population sizes, low genetic variability, and little or no exposure to highly acidic conditions? It is these organisms that may prove most vulnerable.–Anne M. Rosenthal

A video by Stephen Palumbi and Eric Sanford, UC Davis (Bodega Marine Laboratory) on the Microdocs YouTube channel, describes the experiment in lay terms and shows the set-up:
https://www.youtube.com/watch?v=wDcDqULXDOE

References:

Melissa H. Pespeni (now a post-doctoral researcher at Indiana University) web site: 

http://mypage.iu.edu/~mpespeni/Pespeni.html/Home.html

Pespeni, M.H. et al., 2013, Evolutionary change during experimental ocean acidification. PNAS 110(17): 6937-6942. PDF available through Pespeni website.

Pespini, M.H. as quoted in Karoi, L., April 17, 2013 blog post, Evolve and Adapt – Sea Urchins' Climate Change Strategy, take part.com

Buchsbaum, R., et al. 1987. Animals without backbones, 3rd edition. University of Chicago Press, Chicago.

Durham, J.W., et al. 1980. Echinoidea: The Sea Urchins in Intertidal invertebrates of California by Morris, R.H., Abbott, D.P., and E.C. Haderlie, Stanford University Press, Stanford, CA

A Native: The Yellow-faced Bumblebee

A yellow-faced bumble bee comes in for a landing on a California poppy. Photograph copyright Anne M. Rosenthal.

One of our most recognizable native bees, the yellow-faced bumble bee, Bombus vosnesenskii, has a yellow face and a narrow yellow band at the end of the abdomen. In early spring, you may spot the huge female flying slowly just above the ground, searching for her nest site. The sterile workers are much smaller, although they vary quite a bit in size. The first generation of workers is raised by the queen, with subsequent workers raised by the initial brood. Males and new queens are produced in fall, followed by mating, then hibernation by the new queens.

This yellow-faced bumble bee is gathering pollen from a rose flower. Pollen is carried on the back leg by queens and workers. Photograph copyright Anne M. Rosenthal.

Dew weights down a yellow-faced bumble bee early in the morning. Photograph copyright Anne M. Rosenthal.

As night falls, a yellow-faced bumble bee, too cold to fly, hooks itself to a plant. Photograph copyright Anne M. Rosenthal.


Reference:

Powell, J. and C. Hogue. 1979. California Insects. University of California Press, Berkeley.

Robbing Nectar

A female California carpenter bee, Xylocopa californica, distinguished by the bluish metallic reelections on her abdomen and smoky brown wings, drinks nectar from a well drilled at the base of a sage flower. Note an additional well in the base of the second flower. Photograph copyright Anne M. Rosenthal.

Flowers produce nectar to lure pollinators inside. When entering to partake, an insect brushes past the flower's anthers, which bear the pollen. Some pollen sticks to the insect and is transported on to the next flower. To put it succinctly, nectar is payment for a job, and that job is pollination.

But what if you're an insect too big to crawl inside a nectar-bearing flower – perhaps many times too big? Carpenter bees solve this problem by drilling a well through the base of the flower. In other words, they steal the nectar instead of working for it.

A male mountain carpenter bee, Xylocaopa tabaniformis, drinks from a flower well. Note the bald spot on the bee's middle section (the thorax), likely caused by a mite – possibly the minuscule red flat patch near the line of remaining hairs. Worn wings indicate this bee is a senior citizen. Photograph copyright Anne M. Rosenthal.

The chewing apparatus of the female California carpenter bee in silhouette. Photograph copyright Anne M. Rosenthal.

California carpenter bees come equipped with formidable mouthparts, used by females to excavate nesting tunnels. Since carpenter bees often excavate in fences or other structures, they bear a mixed reputation of pollinator and pest.

Opened by a woodpecker searching for larvae, this California carpenter bee nesting tunnel in a redwood fence contains individual nest cells separated by disks of cemented wood bits. Photograph copyright Anne M. Rosenthal; taken on the property of Irene Brown, PhD., with permission.


Chewing through a flower is child's play by comparison. However, it's still a certain amount of work, and carpenter bees often scout for predrilled nectar wells rather than making new ones. Other insects, such as honey bees, may sip from the wells when the carpenters are not around.

Despite cheating this sage flower by robbing nectar, a female California carpenter bee has collected pollen from – and in so doing pollinated – other flowers. She carries the pollen in short stiff hairs, known collectively as a pollen brush, on her hind legs. Photograph copyright Anne M. Rosenthal.

References:

Milne, L. and M. 1980. National Audubon Society field guide to North American insects and spiders. Alfred A. Knopf, New York.

Powell, J. and C. Hogue. 1979. California insects. University of California Press, Berkeley.

Sudden Oak Death: Deadly Invasive Continues Sweep

Mature coast live oaks may become a relic of the past; they are susceptible to a single-celled, infectious organism called a water mold. Coast live oaks are especially susceptible when situated close to California bay laurel trees.

Leaving a million dead trees in its wake, the epidemic of Sudden Oak Death (SOD) in California continues onward. How did this disease, first noted in Marin County tan oaks less than 20 years ago, take such a swift and massive toll on the central California landscape?

Speaking in November of 2012 at Stanford's Jasper Ridge Biological Preserve, Stuart Koretz, MD, PhD, addressed this topic from an epidemiological and general scientific point of view.

An infectious agent, a susceptible population, a mode of transmission, and a reservoir of infection are all part of the Sudden Oak Death epidemic, noted Koretz, who has reviewed considerable literature on the subject and has been a participant in the citizen scientist effort to support monitoring and research.

Grouped with organisms called "water molds" and classified as Oomycetes in kingdom Protoctista, the infectious single-celled Phytophthora ramorum bears some characteristics typical of fungi, for example filamentous growth.  However, these similarities are likely a result of convergent evolution rather than proximity on the tree of life.  In other words, subject to similar environmental challenges over evolutionary time, the water molds found some of the same survival solutions that fungi did, thus developing similar structures.

A healthy evergreen forest with mature oaks in abundance.

A mind-boggling number of diverse plant species are infected by P. ramorum, ranging from the coast redwood (Sequoia sempervirens) – the world's tallest tree – to the pungent broadleaf tree California bay laurel (Umbellularia californica) and understory plants such as Rhododendron, sp., poison oak (Toxicodendron diversilobum), and wood fern (Dryopteris arguta). Importantly, the pathogen also infects key components of oak and mixed woodlands throughout Central California—tanbark oaks (Lithocarpus densiflora) and two of the oaks in the red oak lineage (subgenus Erythrobalanus), coast live oak (Quercus agrifolia) and black oak (Quercus kelloggii).

But while these oaks have taken a big hit, most other infected species show more subtle effects. For example, infected redwoods may display dead needles and sometimes entirely dead twigs, while infected bays may exhibit leaves with brownish tips. In contrast, the trunks of infected oaks become girdled with cankers. This affects vascular cambium – the growth layer of a tree trunk – as well as the transport systems for sap (phloem) and water (xylem), which are located near the periphery of the trunk close to the bark (as opposed to in the interior of the tree, which basically serves structural purposes). Thus the rapidly reproducing single-celled water mold may fell, within just a few years of initial infection, grand, well-established trees that grew for decades or even centuries.

The first clues that an epidemic was underway surfaced in Marin County in 1995, according to the synopsis presented by Koretz. Tanoaks were dying, typically with oozing cankers towards the base of the trunk. Bark and ambrosia beetles drilling the dead and moribund trees left telling piles of sawdust; black golf balls of hypoxylon fungus, a signature of tree death, studded the limbs. By 1997, coast live oaks were also declining, bearing similar hallmarks of infection.

The disease became visible in black oaks, as well as spreading geographically, in 1998, leading to a major collaborative effort to identify the culprit organism, according to Koretz. This joint effort involved the University of California (UC), Berkeley, UC Davis, and the USDA Forest Service, among many others. By 2001, Marin County had declared a state of emergency, and task forces had formed both in California and Oregon (where there was now a localized "pinpoint" infection). Scientists showed definitively that the causal organism was Phytophthora ramorum by fulfilling Koch's postulates: The organism was present in every case examined, it was isolated in pure culture, inoculation into healthy plant tissue produced the same disease, the organism was then isolated from the experimentally infected plants.

Continued investigation revealed a complex epidemiology. Researchers determined that the original source was most likely infected nursery stock possibly originating from a foreign location. Many plants were involved, including several tree species as well as understory herbs, shrubs, and vines, ranging across plant families as diverse as ferns and heaths. Most, though symptomatic, survived infection, at least as mature plants. But some of these living reservoirs shed large numbers of infectious asexual spores. 

The California bay laurel turned out to be a major source of the infection, both harboring the water mold and shedding copious quantities of spores after warm spring rains. Proximity of bays to coast live oaks in Coast Range evergreen forests spread the infection through spore-loaded rain drip onto oak tree trunks, where inoculum stuck to the rough bark. While the infection did not move easily from one coast live oak to another, tanoaks both died of the infection and spread the infectious agent.

Researchers and agencies, with the assistance of citizen scientist volunteers, continue to monitor the infection, through ground and aerial surveys. In "stream-baiting," uninfected plant material is exposed to flowing waters potentially transporting the water mold from upstream watersheds. Strict controls are now in place on moving infected wood or soil, and on the distribution of nursery stock. –Anne M. Rosenthal

To view a map of the infection, see the following web site:

 http://www.oakmapper.org 

A general reference, including photos of infected plants, is available through the California Oak Mortality Talk Force:

 http://www.suddenoakdeath.org/