Robert P. Creed

Direct and Indirect Effects of Crayfish Grazing in a Stream Community

In surveys and experiments in a Michigan stream I found that large crayfish (Orconectespropinquus) can indirectly facilitate epilithic diatoms and sessile, grazing insects by virtually excluding a filamentous alga (Cladophora glomerata) from deep water habitats. In shallow (< 20 cm) habitats, Cladophora cover and ash-free dry biomass usually exceeded 75% and 50 g/m2, respectively. In deep habitats (20-50 cm), Cladophora cover rarely exceeded 10% and ash-free dry biomass was usually <3 g/m2. Mean densities of large crayfish in deep water (3-11 individuals/m2) were 3-20 x greater than their densities in shallow water. Two field experiments were conducted to determine if large crayfish were responsible for the reduced abundance of Cladophora in deep water. In the first experiment, depth and current velocity were held constant for all substrata, and crayfish were excluded from half of the substrata. As physical factors such as current velocity and light may vary with water depth, a second experiment was conducted that compared the effect of substrata depth vs. crayfish grazing on Cladophora abundance. In both experiments, Cladophora biomass was at least 10 x greater on substrata which were not grazed by large crayfish. In the second experiment, substratum depth did not have a significant effect on Cladophora abundance. The results of both experiments demonstrated that grazing by large crayfish was the primary mechanism generating the pattern of Cladophora distribution observed in Augusta Creek. The virtual exclusion of Cladophora from deep water habitats by large crayfish can indirectly facilitate epilithic diatoms and sessile, grazing insects that consume these diatoms. Diatoms and sessile, insect grazers were found to be less abundant beneath Cladophora mats in field experiments. Total diatom abundance on substrata without a Cladophora canopy was 20 x that of substrata with a Cladophora canopy. Two sessile, grazing insects (Psychomyia flavida and Leucotrichia pictipes) were 2-3 x more abundant on substrata which did not have heavy Cladophora cover. These results suggest that crayfish are a keystone consumer in this stream community, but the effect is habitat specific and related to crayfish body size.

USE OF A NATIVE INSECT AS A BIOLOGICAL CONTROL FOR AN INTRODUCED WEED

We have evaluated the potential of a North American aquatic weevil, Euhr- ychiopsis lecontei, to serve as an agent of biological control for an exotic weed, Eurasian watermilfoil (Myriophyllum spicatum), which is currently found throughout much of the United States and in some southern provinces of Canada. We have found this weevil on M. spicatum in lakes where populations of the exotic weed have declined. We introduced weevils into enclosures in two lakes dominated by M. spicatum. In both lakes there was 50% less M. spicatum biomass in enclosures with weevils than in enclosures without weevils. Also, in control enclosures, M. spicatum formed a canopy on the water surface as it did outside the enclosures, while there was no plant canopy in any of the weevil enclosures. In laboratory feeding trials we quantified the effects of weevils on ten native aquatic plants including a native watermilfoil, Myriophyllum sibiricum. Weevils did not have a significant effect on the increase in plant length or final dry mass of any native plant, however the weevils did feed on the native watermilfoil. All native plants added new leaves, leaf whorls, or side branches under all weevil densities. The results from these studies suggest that a North American insect may be a suitable control agent for this introduced aquatic weed. Native biological control agents, when they can be found, offer potential advantages over classical biological control agents; they may have little impact on non-target native species that have coexisted with the control agent, and may save the time and expense of foreign research and quarantine procedures.

Weevils and Watermilfoil: Did a North American Herbivore Cause the Decline of an Exotic Plant?

The Eurasian watermilfoil (Myriophyllum spicatum) population in Brownington Pond, Vermont, declined between 1986 and 1989. Watermilfoil covered ≈10-11 ha of the littoral zone in 1986. Less than 0.5 ha remained in 1989. An herbivorous weevil (Euhrychiopsis lecontei), which is native to North America, was found associated with this watermilfoil population and we hypothesized that this weevil played a role in the decline. We monitored watermilfoil and E. lecontei populations in Brownington Pond from 1990 through 1992 by (1) mapping the location and extent of beds in the pond, and (2) determining watermilfoil biomass along permanent transects. The abundance of weevil eggs, larvae, pupae, and adults were monitored by sampling individual watermilfoil stems. Watermilfoil cover increased to ≈ 2.5 ha by 1991 and then declined again to ≈1 ha by 1992. The reduction in watermilfoil biomass from 1991 to 1992 ranged from 4- to 30-fold depending on location. Mean weevil abundance increased from 1990 (<1/stem) through early 1992 (3-4/stem) and then began to decline. The number of weevil eggs/stem also peaked in early 1992 and then declined. These survey results are consistent with the hypothesis that the weevil played an important role in producing both observed declines. The effect of weevils on watermilfoil was evaluated in two experiments. In an aquarium experiment, we found that the viability of stem fragments damaged by weevils was reduced compared to stem fragments without weevil damage. Watermilfoil commonly spreads by producing fragments so the spread of watermilfoil beds by fragmentation may be reduced when weevil abundances are high. In a pond enclosure experiment, weevils suppressed the production of new watermilfoil biomass. The biomass of lateral stems and roots of watermilfoil plants damaged by weevils was significantly less than those of control plants. There was no significant difference in the biomass of the stems originally planted in the enclosures. Weevil damage did have a negative effect on the buoyancy of these original stems, however. These experimental results also support the hypothesis that this native weevil played an important role in the two watermilfoil declines observed at Brownington Pond.

Branchiobdellid annelids and their crayfish hosts: are they engaged in a cleaning symbiosis?

Abstract. Branchiobdellid annelids and their freshwater crayfish hosts are generally thought to have a commensal relationship. Branchiobdellids of the genus Cambarincola exploit their hosts through a variety of mechanisms; however, an effect of branchiobdellids on crayfish has not been conclusively demonstrated. We investigated whether branchiobdellids positively affect the host crayfish Cambaruschasmodactylus in the New River, North Carolina. In a laboratory experiment, we placed 0, 3, or 6 branchiobdellids on C. chasmodactylus and observed a significant effect of branchiobdellid presence on both growth and mortality of host crayfish; crayfish with branchiobdellids exhibited faster growth and lower mortality with increasing branchiobdellid density. A tracer experiment demonstrated that branchiobdellids feed on items found in the branchial chamber of C. chasmodactylus. We hypothesize that such feeding activity by branchiobdellids reduces fouling of crayfish gills by epibionts and particulate matter and could lead to the reduced mortality and increased growth rates observed in the laboratory experiment. Specifically, Cambarincola may improve the ventilatory and excretory fitness of C. chasmodactylus by cleaning gill filaments. Field data support this hypothesis by demonstrating that branchiobdellids are found disproportionately at sites proximal to the branchial chamber in the New River. This study provides evidence that the relationship between C. chasmodactylus and Cambarincola may be a cleaning symbiosis, at least in environments where gill fouling is a problem for C. chasmodactylus.

The fine line between mutualism and parasitism: complex effects in a cleaning symbiosis demonstrated by multiple field experiments

Ecological theory and observational evidence suggest that symbiotic interactions such as cleaning symbioses can shift from mutualism to parasitism. However, field experimental evidence documenting these shifts has never been reported for a cleaning symbiosis. Here, we demonstrate shifts in a freshwater cleaning symbiosis in a system involving crayfish and branchiobdellid annelids. Branchiobdellids have been shown to benefit their hosts under some conditions by cleaning material from host crayfish’s gill filaments. The system is uniquely suited as an experimental model for symbiosis due to ease of manipulation and ubiquity of the organisms. In three field experiments, we manipulated densities of worms on host crayfish and measured host growth in field enclosures. In all cases, the experiments revealed shifts from mutualism to parasitism: host crayfish growth was highest at intermediate densities of branchiobdellid symbionts, while high symbiont densities led to growth that was lower or not significantly different from 0-worm controls. Growth responses were consistent even though the three experiments involved different crayfish and worm species and were performed at different locations. Results also closely conformed to a previous laboratory experiment using the same system. The mechanism for these shifts appears to be that branchiobdellids switched from cleaning host gills at intermediate densities of worms to consuming host gill tissue at high densities. These outcomes clearly demonstrate shifts along a symbiosis continuum with the maximum benefits to the host at intermediate symbiont densities. At high symbiont densities, benefits to the host disappear, and there is some evidence for a weak parasitism. These are the first field experimental results to demonstrate such shifts in a cleaning symbiosis.

The effects of 2 coexisting crayfish on an Appalachian river community

Abstract Crayfish can act as keystone species and ecosystem engineers in small streams, but their effects in large rivers are not well known. Two species of crayfish, Orconectes cristavarius and Cambarus chasmodactylus, coexist in the South Fork of the New River in western North Carolina. We used gut-content analyses and an enclosure–exclosure experiment to investigate the influence of both species of crayfish on sediment accumulation and benthic invertebrates. Crayfish guts contained mostly sediment and vegetative detritus. However, C. chasmodactylus guts contained significantly more detritus and animal matter than O. cristavarius guts, and O. cristavarius guts contained significantly more sediment than C. chasmodactylus guts. In the field experiment, sediment volume was lower in open baskets and cage controls, which were exposed to crayfish and benthic-feeding fish, than in enclosures containing only crayfish. Sediment volume was highest in fish/crayfish exclosures. Despite their effect on sediment accumulation, crayfish did not significantly affect the density of any invertebrate taxon. No clear relationship was found between chironomid density and enclosure–exclosure treatment, but chironomid density was positively correlated with sediment volume. Damselflies (Calopteryx maculata) tended to be more abundant in crayfish enclosures than in open treatments and cage controls, and cyclopoid copepods tended to be more abundant in O. cristavarius enclosures than C. chasmodactylus enclosures. The significant differences in the diets of the 2 species of crayfish were not associated with differences in their effects on invertebrates. Our results suggest that these 2 species of crayfish may be functionally redundant in this community, despite differences in diet. Furthermore, the lack of pronounced crayfish effects on invertebrate taxa suggests that the effects of crayfish may not be as strong in large rivers as in small streams.

Predator transitions in stream communities: a model and evidence from field studies

Abstract The role of predators (particularly top predators such as fish) in structuring stream communities has been debated for 2 decades. Much of the debate may have been caused by the lack of a conceptual framework for evaluating predator effects in stream communities. First, I propose a general conceptual model of the factors (abiotic, such as stream permanence and disturbance regime; biotic, such as predation) that can influence community structure, and the conditions in which these various factors would be expected to be important. Hydrologic permanence and disturbance transitions separate streams where abiotic factors are most important in determining community structure from streams with relatively benign disturbance regimes where predation may be more important. Second, I focus on the potential effect of predators in perennial streams with relatively benign disturbance regimes. Such streams are divided longitudinally into sections where different types of predators might be important in determining community structure. Large invertebrates (stoneflies, dragonflies, shrimp, and crayfish) and salamanders may be the dominant benthic predators affecting species composition in small perennial fishless streams. A transition from invertebrate- and amphibian-dominated to fish-dominated systems may occur in larger, downstream sections (predator transition 1). In addition, longitudinal transitions in fish-assemblage structure from upstream tributaries to downstream main-channel fish assemblages (predator transition 2) may affect community structure. I present evidence supporting the above model and suggest experimental approaches to test the model. This conceptual framework may help in understanding the role of specific predators in determining prey distributions in many stream communities.

Abiotic factors, competition or predation: what determines the distribution of young crayfish in a watershed?

In the headwaters of the New River in western North Carolina, the dominant crayfish species changes with increasing stream size. One transition occurs between third- and fourth-order streams. Cambarus chasmodactylus is the dominant species in third-order tributaries. Orconectes cristavarius is the dominant species in the fourth-order South Fork of the New River. While adult C. chasmodactylus are present in the South Fork, the young-of-the-year (YOY) of this species are absent despite evidence of reproduction. In this study we evaluated the factors that may be responsible for the absence of C. chasmodactylus YOY from the South Fork. A field experiment was used to evaluate the role of abiotic factors and competition with YOY O. cristavarius. There was no significant effect of either of these factors on mortality or growth of C. chasmodactylus YOY. The growth rate of O. cristavarius was 3× faster than that of C. chasmodactylus in this experiment. Since neither abiotic factors nor competition appeared responsible for the exclusion of C. chasmodactylus YOY from the South Fork we evaluated the potential importance of selective predation by rock bass (Ambloplites rupestris), a fish species that is common in the South Fork but virtually absent in the tributaries. In a laboratory experiment, C. chasmodactylus YOY experienced significantly higher mortality than O. cristavarius YOY in the presence of rock bass. Field observations and a laboratory experiment suggest that the two crayfish species differ in their anti-predator behaviors. Cambarus chasmodactylus was less likely to swim when initially disturbed and swam shorter distances than O. cristavarius. The differences in escape behavior and growth rate may contribute to the differences in the vulnerability of the two species to rock bass predation. Our results suggest that intense predation pressure exerted by the rock bass may contribute to the virtual exclusion of C. chasmodactylus YOY from the fourth-order South Fork.

Preventing overexploitation in a mutualism: partner regulation in the crayfish–branchiobdellid symbiosis

For a symbiosis to be a mutualism, benefits received must exceed costs incurred for both partners. Partners can prevent costly overexploitation through behaviors that moderate interactions with the other symbiont. In a symbiosis between crayfish and branchiobdellidan annelids, the worms can increase crayfish survival and growth by removing fouling material from the gills. However, overexploitation by the worms is possible and results in damage to host gills. We used behavioral observations to assess the degree to which two species of crayfish (Cambarus chasmodactylus and Orconectes cristavarius) use grooming to moderate their interaction with branchiobdellids. We found that grooming could effectively reduce worm numbers, and the proportion of total grooming directed at worms differed between crayfish species and as a function of worm number. O. cristavarius increased grooming in response to the addition of a single worm, while C. chasmodactylus only increased grooming in response to ten worms. These differences in the number of worms that trigger grooming behavior reflect differences between crayfish species in field settings. We also assessed whether antibacterial compounds in circulating crayfish hemolymph could limit bacterial gill fouling. O. cristavarius hemolymph inhibited some test bacteria more effectively than C. chasmodactylus did. Differences in the antibacterial properties of crayfish hemolymph may therefore help explain differences in both worm-directed grooming and worm loads in the field. We conclude that crayfish can use grooming to reduce worm numbers, which could lower the potential for gill damage, and that the level of grooming varies between crayfish species.

Servants, scoundrels, and hitchhikers: current understanding of the complex interactions between crayfish and their ectosymbiotic worms (Branchiobdellida)

Abstract.  Astacoidean crayfishes serve as hosts to obligate ectosymbiotic annelids called branchiobdellidans. Branchiobdellidans can act either as mutualistic cleaners or as ectoparasites and can have strong effects on crayfish growth and survivorship. This potentially vital aspect of crayfish biology has gone largely unexplored until recently. We reviewed the current state of knowledge regarding this symbiosis and examined factors that contribute to variability in the effects of branchiobdellidans on crayfish. We show that branchiobdellidans affect crayfish in various ways depending on branchiobdellidan species, abundance, and ecological context. We also discuss evidence for regulatory controls that crayfish exert over their symbionts and symbiont–host preferences. Last, we evaluate the utility and challenges of using the crayfish–branchiobdellidan association as a model system for ecological and evolutionary research and point to promising areas for future study. Further investigations of the complex interactions between crayfish and their ectosymbionts will greatly advance the field of crayfish biology and offer many exciting opportunities for the study of symbioses.