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

Homemaker, Lovemaker, Engineer

A blue pincher emerging from its burrow in the rhizome mat. The green at the edge is likely MPB, which might collect in this relatively protected area.

While they are not the most attractive of crabs, nor of interest to any fishery, Thalamita crenata, or the "blue pincher" is numerically the most dominant crab in the fishpond. I am interested in it because it seems to have no problem living in concert with the toughest invaders. Blue pinchers can be found burrowing in the mangrove rhizome mat, or feeding within the Gracilaria canopy. They are an excellent example of how structure-forming species (mangrove and Gracilaria) can influence community structure, and also a lesson: species can be ecosystem engineers not just by increasing habitat complexity by building structure, but also by decreasing it.

Two blue pincher crabs mating at the ocean break.

Generally, invasive species that increase habitat complexity also increase abundance and/or diversity in invaded areas. Unlike invasive pigs (Sus scrofa) and other terrestrial invaders which decrease habitat complexity in native forests, organisms like limu and burrowing crabs create more diverse habitat, which can make room for more native or alien species. Knowledge of these community effects can be helpful for predicting responses to new invasions, but the scales of invasion and community interaction are important in determining what these responses are (Crooks 2002). Additionally, the life histories of the involved species can also affect community responses (e.g., the snail Littorina littorea transforms muddy habitat into what is essentially a rocky shore, but native species which favor rocky habitat do quite well with the modification). In a place like Hawaii where the preservation of native diversity is a high priority, knowing the effects of certain invaders on the ecosystem is a powerful conservation tool.

Crooks, J. (2002). Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers Oikos, 97 (2), 153-166 DOI: 10.1034/j.1600-0706.2002.970201.x

Alien Babies: To'au in He'eia Mangroves

While I was seining with the LAIP interns this past summer, we came across some interesting fish living near the mangroves. While some of the fish and nearly all the invertebrates we've seen are species that may spend their entire lives in the pond (the half-spotted goby, for example, or Podopthalmus vigil, the Hawai'ian swimming crab), others are transient. Many Hawai'ian fishponds are strategically placed at the mouths of streams because highly productive, protected estuaries are important nursing grounds. As the fishpond wisdom goes, tiny fish and food go in, larger fish can't escape, and voilà: a productive and low-impact fishery. Fishponds like He'eia can attract juvenile reef fish in addition to traditional food fish, making for a diverse and colorful community of juveniles. Above is a juvenile to'au (Lutjanus fulvus) we caught in the mangroves by one of the river makaha. To'au are an alien snapper species found in abundance on Hawai'ian reefs. They are efficient at colonizing new areas (genetic evidence here) though they are not necessarily invasive; more on this important distinction later.

Mahalo nui to Jack Randall, Senior Ichthyologist at the Bishop Museum for help with the ID.

More on L. fulvus and its range in the Indo-Pacific:
Gaither, M., Toonen, R., Robertson, D., Planes, S., & Bowen, B. (2009). Genetic evaluation of marine biogeographical barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus) Journal of Biogeography, 37 (1), 133-147 DOI: 10.1111/j.1365-2699.2009.02188.x

Back to Bacteria: A "Big Rotten Loofah"

Mangrove detritus pulled out of a sediment core at the south edge of the pond.

The surface of a rhizome mat where mangrove overstory was removed four years ago.

The surface is soft, and decomposing root fibers protrude into the water. The stringy fragments in the foreground are worm waste.

More on the mangrove story: This Tuesday we took sediment cores from two areas where mangrove overstory (prop roots and trunks) were cut down in 2007 and 2008. In these areas, dead stumps still stick out of the mud, and a thick, fibrous root mat stabilizes the sediments. Even though the overstory was removed four years ago, the rhizome mat is still intact, making it relatively easy to walk on. In most areas, however, it's riddled with burrows. This brings up an important question-- what is the role of these burrowing and other bioturbators in breaking down the rhizome mat? Importantly, does mangrove-based carbon enter the food web more readily when mangrove mat is decomposing, and exposed to wind-mixed water, than when mangroves are actively building fresh (tough, tannin-rich) rhizome? This is a food web approach to mangrove community effects, and a very interesting one. Previous studies suggest that short term carbon cycling in mangrove sediments is dominated by bacteria at first, then macrofauna (crustaceans, worms, mollusks, nematodes), and then back to bacteria (Sweetman et al. 2010). Additionally, in living mangroves in Kaneohe Bay, mangrove-based carbon isn't taken up into the food web (Demopoulos et al. 2007). Perhaps when crabs and other burrowers are more actively breaking down mangrove material, there are more opportunities for mangrove carbon to subsidize the local food web. This is a question for stable isotopes.

Sweetman, A., Middelburg, J., Berle, A., Bernardino, A., Schander, C., Demopoulos, A., & Smith, C. (2010). Impacts of exotic mangrove forests and mangrove deforestation on carbon remineralization and ecosystem functioning in marine sediments Biogeosciences Discussions, 7 (2), 2631-2671 DOI: 10.5194/bgd-7-2631-2010

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