Kaitlin J. Farrell

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.

Salting our freshwater lakes

Significance In lakes, chloride is a relatively benign ion at low concentrations but begins to have ecological impacts as concentrations rise into the 100s and 1,000s of mg L−1. In this study, we investigate long-term chloride trends in 371 freshwater lakes in North America. We find that in Midwest and Northeast North America, most urban lakes and rural lakes that are surrounded by >1% impervious land cover show increasing chloride trends. Expanding on this finding, thousands of lakes in these regions are at risk of long-term salinization. Keeping lakes “fresh” is critically important for protecting the ecosystem services freshwater lakes provide, such as drinking water, fisheries, recreation, irrigation, and aquatic habitat. The highest densities of lakes on Earth are in north temperate ecosystems, where increasing urbanization and associated chloride runoff can salinize freshwaters and threaten lake water quality and the many ecosystem services lakes provide. However, the extent to which lake salinity may be changing at broad spatial scales remains unknown, leading us to first identify spatial patterns and then investigate the drivers of these patterns. Significant decadal trends in lake salinization were identified using a dataset of long-term chloride concentrations from 371 North American lakes. Landscape and climate metrics calculated for each site demonstrated that impervious land cover was a strong predictor of chloride trends in Northeast and Midwest North American lakes. As little as 1% impervious land cover surrounding a lake increased the likelihood of long-term salinization. Considering that 27% of large lakes in the United States have >1% impervious land cover around their perimeters, the potential for steady and long-term salinization of these aquatic systems is high. This study predicts that many lakes will exceed the aquatic life threshold criterion for chronic chloride exposure (230 mg L−1), stipulated by the US Environmental Protection Agency (EPA), in the next 50 y if current trends continue.

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.u2003 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.

Baseflow physical characteristics differ at multiple spatial scales in stream networks across diverse biomes

ContextSpatial scaling of ecological processes is facilitated by quantifying underlying habitat attributes. Physical and ecological patterns are often measured at disparate spatial scales limiting our ability to quantify ecological processes at broader spatial scales using physical attributes.ObjectiveWe characterized variation of physical stream attributes during periods of high biological activity (i.e., baseflow) to match physical and ecological measurements and to identify the spatial scales exhibiting and predicting heterogeneity.MethodsWe measured canopy cover, wetted width, water depth, and sediment size along transects of 1st–5th order reaches in five stream networks located in biomes from tropical forest to arctic tundra. We used hierarchical analysis of variance with three nested scales (watersheds, stream orders, reaches) to identify scales exhibiting significant heterogeneity in attributes and regression analyses to characterize gradients within and across stream networks.ResultsHeterogeneity was evident at one or multiple spatial scales: canopy cover and water depth varied significantly at all three spatial scales while wetted width varied at two scales (stream order and reach) and sediment size remained largely unexplained. Similarly, prediction by drainage area depended on the attribute considered: depending on the watershed, increases in wetted width and water depth with drainage area were best fit with a linear, logarithmic, or power function. Variation in sediment size was independent of drainage area.ConclusionsThe scaling of ecologicallyxa0relevant baseflow physical characteristics will require study beyond the traditional bankfull geomorphology since predictions of baseflow physical attributes by drainage area were not always best explained by geomorphic power laws.

Continental-scale decrease in net primary productivity in streams due to climate warming

An increase in stream temperature leads to a convergence of metabolic balance, overall decline in net ecosystem productivity, and higher CO2 emissions from streams, according to analyses of temperature sensitivity of stream metabolism across six biomes.AbstractStreams play a key role in the global carbon cycle. The balance between carbon intake through photosynthesis and carbon release via respiration influences carbon emissions from streams and depends on temperature. However, the lack of a comprehensive analysis of the temperature sensitivity of the metabolic balance in inland waters across latitudes and local climate conditions hinders an accurate projection of carbon emissions in a warmer future. Here, we use a model of diel dissolved oxygen dynamics, combined with high-frequency measurements of dissolved oxygen, light and temperature, to estimate the temperature sensitivities of gross primary production and ecosystem respiration in streams across six biomes, from the tropics to the arctic tundra. We find that the change in metabolic balance, that is, the ratio of gross primary production to ecosystem respiration, is a function of stream temperature and current metabolic balance. Applying this relationship to the global compilation of stream metabolism data, we find that a 1u2009°C increase in stream temperature leads to a convergence of metabolic balance and to a 23.6% overall decline in net ecosystem productivity across the streams studied. We suggest that if the relationship holds for similarly sized streams around the globe, the warming-induced shifts in metabolic balance will result in an increase of 0.0194u2009Pg carbon emitted from such streams every year.

Reduced Densities of Ectosymbiotic Worms (Annelida: Branchiobdellida) on Reproducing Female Crayfish

Abstract n Cleaning symbioses provide net benefits by improving each partners fitness. Ectosymbiotic Cambarincola spp. (branchiobdellidans) can increase growth and survival of Cambarus chasmodactylus (New River Crayfish), but the nature of the symbiosis might change with female reproductive state because brooding offspring (eggs, young) and worms inhabit the same surfaces. Here, we present the results of field surveys that examined whether the number and location of branchiobdellidans on New River Crayfish varies as a function of female crayfish reproductive state. Reproducing female New River Crayfish had fewer total worms, an absence of cocoons, and a relatively greater proportion of worms on lateral body surfaces than non-reproducing crayfish. The altered distribution and reduced abundance of worms suggest that the symbiosis changes with female reproductive status, but additional experiments will be needed to identify the mechanism responsible.

A lake classification concept for a more accurate global estimate of the dissolved inorganic carbon export from terrestrial ecosystems to inland waters

The magnitude of lateral dissolved inorganic carbon (DIC) export from terrestrial ecosystems to inland waters strongly influences the estimate of the global terrestrial carbon dioxide (CO2) sink. At present, no reliable number of this export is available, and the few studies estimating the lateral DIC export assume that all lakes on Earth function similarly. However, lakes can function along a continuum from passive carbon transporters (passive open channels) to highly active carbon transformers with efficient in-lake CO2 production and loss. We developed and applied a conceptual model to demonstrate how the assumed function of lakes in carbon cycling can affect calculations of the global lateral DIC export from terrestrial ecosystems to inland waters. Using global data on in-lake CO2 production by mineralization as well as CO2 loss by emission, primary production, and carbonate precipitation in lakes, we estimated that the global lateral DIC export can lie within the range of 0.70−0.31+0.27

Dynamic modeling of organic carbon fates in lake ecosystems

{0.70}_{-0.31}^{+0.27}