We're Moving

I've decided to move Fishpond Fever to another blog host. The new format is more open and flexible, and may be more pleasing to the eye. The new site is http://fishpondfever.wordpress.com/. New posts from now on will be posted there. Check it out!

Dead, Alive, or Excreted: The Mysterious Role of Detritus in Food Webs

Suppose I ate a moldy fish, and my friend ate a fresh one. Though both food items are fish, food web ecologists would probably call my friend's meal "fish" and mine "detritus." Detritus is a catch-all term for dead plant tissue (e.g. leaf litter, dead wood, dead algae), dead animal tissue, feces, mucus, and even things exuded from plants and cells like nectar or extracellular matrix. Particles can vary in size and chemical composition. Detritus is often in some state of decomposition, so it is hard to tell exactly what it is, or where it came from.

A food web in which detritus is a nutrient source can potentially support more diversity, longer food chains, and larger predator biomass than one based only on living material (Hairston & Hairston 1993). It can subsidize the diets of consumers who feed mainly on living material, and it can provide dissolved nutrients to producers (like phytoplankton). Detritus can also be an avenue by which invasive species affect energy flow in native systems, sometimes to the benefit of natives (see Wolkovich 2010). However, there has been a separation in ecology between "brown world" (detritus-based) models, and "green world" (primary-production based) models. The most common food web models dwell in green world: they only incorporate living material, such as algae, as nutrient sources. So why is the ecosystem ecology spotlight still on the living?

Moore (2004) attributes this to an early divide between community ecology and ecosystem ecology. Back in the day, community ecology focused on individual organisms, while ecosystem ecology was nutrient-centric, focusing instead on how carbon, nitrogen and phosphorous move through an ecosystem. Detritus ended up in the nutrient-centric category, and since then has rarely been included in "green" food web models.

Taking a nutrient-centric approach to account for detritus makes some sense because detritus is a) made of dead things b) often made of a mixture of those dead things and c) highly variable in its composition. Not accounting for spatial and temporal variability in detritus sources, and simply counting it as a carbon source, is simply easier.
Imagine a pond with algae in it, that is continually dying and being fed on by bacteria, some of which are also continually dying (Lindeman 1942). An herbivorous fish that eats that algae will certainly also be eating some of those bacteria: so how do we know where the fish's nutrients are coming from? Much easier to measure carbon and nitrogen than to sort out where those molecules came from.

But often we want to know nutrient sources, and chemical/nutrient tracers often fail to reveal them. A detritivore's diet is highly variable, even if it eats the same thing every day. Brown muck with cellulose might occur under, say, a mangrove canopy, but the same brown muck will suddenly become loaded with fishy fatty acids if a fish dies under that canopy. Therefore, if you use chemical tracers to determine food sources, the diet of this brown-muck-eating fish still looks highly variable. I have found this in natural carbon isotope abundances from detritivorous crabs: blue pincher crabs with a < 5 m range, sampled at the exact same site on the same day can have very different carbon isotope signatures. Given this kind of data, we don't know whether the crab has been eating plants, live fish, dead fish, or other crabs, or which of these nutrient sources is most important.

One way to overcome this issue is to work with label addition experiments-- these are popular in seagrass and algal ecology, and can at least distinguish whether things are eating living or dead plant matter. Living plants take up nitrogen, so you can label plant material by adding an isotope tracer, like isotopically heavy nitrogen, to your study site. The live plants and algae will take up the tracer, while detrital material (especially if it's washing in from somewhere else, like a stream) will not. Then you can measure consumers to see if they ate labeled material (if they ate something labeled with heavy N, it will show up in their tissue nitrogen values). Compound-specific stable isotope measurements can also track material through detrital loops as well.

The incorporation of detrital variability and green-brown interactions into food web models is only just beginning, though there is promise in compound-specific and stable isotope methods. These advances will be of utmost importance to food web ecologists.

Where green world and brown world collide: mats of benthic microalgae are glued together with detritus, but fish eat the mats indiscriminantly, obtaining nutrients from both detritus and microalgae.

Hairston, Jr., N., & Hairston, Sr., N. (1993). Cause-Effect Relationships in Energy Flow, Trophic Structure, and Interspecific Interactions The American Naturalist, 142 (3) DOI: 10.1086/285546

Moore, J., Berlow, E., Coleman, D., Ruiter, P., Dong, Q., Hastings, A., Johnson, N., McCann, K., Melville, K., Morin, P., Nadelhoffer, K., Rosemond, A., Post, D., Sabo, J., Scow, K., Vanni, M., & Wall, D. (2004). Detritus, trophic dynamics and biodiversity Ecology Letters, 7 (7), 584-600 DOI: 10.1111/j.1461-0248.2004.00606.x

Lindeman, R. (1942). The Trophic-Dynamic Aspect of Ecology Ecology, 23 (4) DOI: 10.2307/1930126

Shelter or Buffet? The Predator Paradox In Mangrove Communities

Samoan crab (Scylla serrata), a predator associated with mangrove forests in Hawaii and other parts of the Pacific. Though alien species in Hawaii, they are not considered a threatening invasive, because they grow slowly and are a popular fishery.

What's in a mangrove? Anoxic, tannin-rich sediments, yes. But there are also predators... quite a few of them. Brian Nakahara, a recently graduated masters student from the Oceanography department at UH found that there are higher abundances of predators inside mangrove forests than on adjacent bare sediments. He also found that predators with smaller sizes tended to inhabit the mangrove canopy, suggesting that even in Hawaii, where mangroves are invasive, predators might use the canopy as nursery habitat. Why is this exciting, you ask?

Well, for one, predators are exciting. They are big and scary and sometimes delicious (see Scylla serrata, above). But they also present an opportunity to challenge a common conception about the functional role of mangroves.

Mangroves provide carbon in the form of leaf litter, and are an efficient sink for heavy metals and nutrient runoff. Though the sediments underneath mangroves are indeed anoxic, they contain a hefty load of organic material, which enters the food web where mangroves are native (Demopoulos 2007). But because of their unique structure, there is also a strong physical component to their influence on marine systems: the surfaces of prop roots are habitat for fouling organisms and prop root structure protects organisms inside the mangrove from large predators. Though mangroves provide habitat for some organisms, they provide food for others.

In terms of predator-prey interactions, the case for mangrove function can be made two ways:

"Mangrove As Shelter": mangrove prop roots increase habitat complexity, which, according to ecological theory, allows more species to co-exist in an area (Levin 1992). It may also impede the ability of larger predators to forage, depending on the density of roots.

"Mangrove As Buffet": On the other hand, the same complex microhabitats in mangroves may provide habitat for many small prey, making mangroves a choicy foraging habitat for predators (Nagelkerken 2004), enhancing predation in mangroves.

The difference between Buffet and Shelter may be one of scale: smaller predators can access more microhabitats within the root structures, while bigger ones can't fit through the door to the buffet. This is an oversimplification, but an important one to bear in mind when examining predator function in the mangroves. My current project seeks to test the relationship between mangroves and the presence of mangrove-associated predators like Samoan crab and tilapia. My primary goal is to characterize the effects of these predators on the infaunal community-- what do these predators eat from the buffet, and how much? This type of question can be answered with a caging experiment in the existing mangroves. Cages that exclude predators will be "predator-free" zones, where infauna are protected from the predators they usually experience. I'll take sediment cores (see "Little Shop of Cores") in caged areas and uncaged areas, and comparisons between them will reveal what predators are eating at the buffet (biodiversity) and how much (biomass).

No experiment would be informative without replication, of course. The LAIP interns and I are finishing the last of 48 predator exclusion cages this week.

An exclusion cage without its lid. The metal band along the bottom sinks into the sediment, anchoring the cage and preventing burrowers from digging under the cage to get inside.

Interns carrying trial cages into the mangrove area.

Demopoulos AW, Fry B, & Smith CR (2007). Food web structure in exotic and native mangroves: a Hawaii-Puerto Rico comparison. Oecologia, 153 (3), 675-86 PMID: 17587064

Levin, S. (1992). The Problem of Pattern and Scale in Ecology: The Robert H. MacArthur Award Lecture Ecology, 73 (6) DOI: 10.2307/1941447

Nagelkerken, I., & van der Velde, G. (2004). Relative importance of interlinked mangroves and seagrass beds as feeding habitats for juvenile reef fish on a Caribbean island Marine Ecology Progress Series, 274, 153-159 DOI: 10.3354/meps274153

Kon, K., Kurokura, H., & Tongnunui, P. (2009). Do mangrove root structures function to shelter benthic macrofauna from predators? Journal of Experimental Marine Biology and Ecology, 370 (1-2), 1-8 DOI: 10.1016/j.jembe.2008.11.001

Just another beautiful day at the fishpond

Whatever Sinks Your Boat: Pests as a Conservation Tool

Close-up of the apical end of a shipworm taken from the He'eia mangroves. Shipworms are not actually worms but bivalves (this picture shows one of the shells, the other is obscured by tissue).

Teredo worms (or shipworms), which are actually bivalves of the family Teredinidae, are legendary in their appetites for ship hulls, wood pilings, or any other wood found in the ocean. Like a clam or any other bivalve, they have two sharp shells on one end, but their long, soft body makes them look more like a worm. These shells make excellent tools for carving burrows in wood, which shipworms line with a calcareous shell. This can make them look like tube-dwelling worms at a glance. The calcareous shell protects the worm from the unstable environment of the wood-- much like humans build tunneling shields when tunneling in unstable substrates. The width of an individual's shell tunnel depends on species, but they can vary within species depending on the degree of crowding in a single piece of wood (Cragg et al. 2009). Members of this family are the primary cause of the characteristic round holes we see in driftwood. Though boat hulls are now usually made with metal or fiberglass, wood hulls used to be a frequent victim of shipworm infestations. The U.S. invests millions of dollars every year in protecting wooden structures from shipworm damage.

There are a few more sides to this voracious group of organisms, however:

1. They are delicious. In parts of Southeast Asia, they are found in abundance in mangrove forests, where humans harvest them for food.
2. They are extremely efficient at recycling decaying wood material and releasing carbon and nitrogen from the mangrove into the surrounding ecosystem. Like termites do on land, they eat wood pulp and digest the cellulose with the help of symbiotic bacteria. This is no trivial task. The tannins that normally protect mangrove from being eaten by herbivores do not deter wood-boring organisms like these, and even healthy mangrove can be damaged by fungi that take refuge in the calcareous tubes (Kohlmeyer 1969). 22-50% of the carbon produced by Rhizophora sp. is stored in woody parts and trunks (as opposed to leaf litter) (Robertson & Daniel 1989). In Rhizophora sp. forests in Australia, 50% of trunk mass decayed after 8 years, and by 4 years after deforestation, trunks were colonized by Teredinids.
3. They are in He'eia Fishpond. LAIP interns discovered high densities of boring bivalves during a POH workday when our task was to dig out mangrove stumps. The patch we dug in was cut down in 2007, and stumps contained live worms and calcareous tubes.

A shipworm and many calcareous tubes found in a mangrove removal area in He'eia Fishpond. The trunk on the left is hollowed out (the spongy interior has been mostly decomposed already), and the periphery bristles with the calcareous tubes of shipworms.

So can a pest be our best hope for returning this system to pre-invasion conditions? How long will it take them, and when they liberate carbon and nitrogen from the mangrove trunks, are there any organisms in the brackish, anoxic mud that can use it? Hawai'i lacks many of the other important species evolved to break down this tough material, but these worms are crucial nutrient cyclers for decomposing mangrove. If we don't have to count exclusively on bacteria to do the job, we may be looking at a faster recovery to pre-invasion conditions.

Cragg, S., Jumel, M., Al-Horani, F., & Hendy, I. (2009). The life history characteristics of the wood-boring bivalve Teredo bartschi are suited to the elevated salinity, oligotrophic circulation in the Gulf of Aqaba, Red Sea Journal of Experimental Marine Biology and Ecology, 375 (1-2), 99-105 DOI: 10.1016/j.jembe.2009.05.014

Kohlmeyer, J. (1969). Ecological notes on fungi in Mangrove forests Transactions of the British Mycological Society, 53 (2) DOI: 10.1016/S0007-1536(69)80058-6

ROBERTSON, A., & DANIEL, P. (1989). Decomposition and the annual flux of detritus from fallen timber in tropical mangrove forests Limnology and Oceanography, 34 (3), 640-646 DOI: 10.4319/lo.1989.34.3.0640

Little Shop of Cores: What Lives in He'eia's Sediments

Behold: The World Beneath Our Tabis! An assortment of worms and amphipods found in sediment cores from mangrove removal areas. The plant fragments are mangrove rhizome fibers.

These invertebrates were found in sediment cores from the edge of the pond, all of them areas were mangroves had been removed (See "Old Scourge, New Questions," January 30th). Some organisms may have been living a few centimeters underneath the sediment surface, while others may have had shallower burrows-- since these samples were depth-integrated, we don't know where these organisms dwell on a finer scale (This can be resolved by sectioning cores in the field; more on this later). While parts of the pond with low salinity are likely to be less species rich, the infauna collected today were collected on the makai side of the pond, closer to the ocean. Whether or not they are more diverse than infauna from the fresher areas of the pond is unknown at this point. If this infaunal community has changed since the mangroves were removed, we may be looking at more "pre-invasion" species which returned when the low-oxygen high-tannin environment of the mangrove sediments was ameliorated by removal. Alternatively, they could be "leftover" anoxia-tolerant species that remained even after mangrove overstory was removed.

Processing a sediment core involves sieving material through 500 µm mesh several times, fixing with formalin, staining with Rose Bengal dye overnight (hence the brilliant magenta of the worms above), and picking through a mixture of mangrove bark, algae fragments, and rhizome pieces to find brightly stained organisms. The search alone takes at least 30 minutes per core. Sorting and identification will be the next step.

What is an ecosystem engineer?

Contents of one clump of G. salicornia from a shallow reef at Ala Moana. These include sponges, ascidians, larval fish, invasive and native algae, and crabs. Other clumps contained juvenile sea cucumbers and other fish species. A recent introduction to the islands has not prevented G. salicornia from becoming both an effective invader and a new habitat for benthic species.

Though I use the term frequently, deciding whether an organism is an ecosystem engineer is difficult. The term "ecosystem engineer" itself is problematic: almost every organism modifies its environment in some way, and in the face of indirect effects, quantifying this modification is nearly impossible. However, this category is useful because it can help us distinguish species which have strong physical impacts on ecosystems from those who affect the community mostly through competition, predation, or other biological pathways. Jones et al. (1997) define ecosystem engineers as "organisms that directly or indirectly control the availability of resources to other organisms by causing physical state changes in biotic or abiotic materials. Physical ecosystem engineering by organisms is the physical modification, maintenance, or creation of habitats." Essentially, ecosystem engineers create, modify, or destroy physical habitat.

Famous examples of ecosystem engineers include beavers, which fell trees and build dams, creating habitat for other organisms and altering patterns of water flow, and prairie dogs, whose burrows create nest habitat for birds. Plant examples abound: terrestrial forests are ecosystem engineers, as are many invasive plants. The cordgrass Spartina anglica has converted soft-bottom nearshore communities in the northeastern US to poorly drained swamps. In Hawai'i, the nitrogen-fixing shrub Morella faya has taken over areas of native forest, and because it fixes nitrogen, has significantly increased nitrogen concentrations in the areas where it has taken over. Mangroves have invaded much of Hawai'i's nearshore habitats and are expected to have significant and varied community impacts (Simberloff 2011). The Invasive alga Gracilaria salicornia alters nutrient concentration and sedimentation and flow rates. Okay, organisms can have physical effects on ecosystems. Why do we need to know whether or not they are engineers, or how much engineering they can do, exactly?

There are at least two reasons: 1) determining the extent of an organisms physical impact on a system is key in deciding whether or not the species will flourish and how it will affect the invaded community. This is particularly important in Hawai'i, which has endured a number of invasions and continues to be on the lookout for new, dangerous potential invasive species. 2) If we study these systems we may be able to build predictive models that tell us not only whether a species will be successful but where it is likely to colonize (Cuddington and Hastings 2004).

Information about invasive engineers can be difficult to sort, and sometimes difficult to find in the first place. But understanding their impacts can be a useful tool for management, and an ecological lesson.

Dinoflagellates and diatoms removed from the surface of a frond of Acanthophora spicifera, another structure-forming alga. A. spicifera is a physical host for microalgae, which grow on its surface and take advantage of localized high nutrient concentrations. In the Caribbean, it hosts Gambierdiscus toxicus, the dinoflagellate that causes Ciguatera Fish Poisoning (CFP). Interactions like these are important and can be vital to human health. (Note: G. toxicus does not grow well in waters with low salinity, so it's unlikely to show up in the fishpond).

Jones, C., Lawton, J., & Shachak, M. (1997). Positive and Negative Effects of Organisms as Physical Ecosystem Engineers Ecology, 78 (7) DOI: 10.2307/2265935

Jones, C., Lawton, J., & Shachak, M. (1994). Organisms as Ecosystem Engineers Oikos, 69 (3) DOI: 10.2307/3545850

Daniel Simberloff (2011). How common are invasion-induced ecosystem impacts? Biological Invasions : 10.1007/s10530-011-9956-3

Cuddington, K. (2004). Invasive engineers Ecological Modelling DOI: 10.1016/S0304-3800(04)00152-8