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.     

Grooming using rotating brushes as a proactive method to control ship hull fouling

Grooming may be defined as the frequent and gentle cleaning of a ship hull coating, when it is in port or idle, to prevent the establishment of fouling. This study assessed the effectiveness of grooming with a five-headed rotating brush system on epoxy, ablative copper and two silicone fouling release (FR) coatings. These coatings were placed under static immersion at Port Canaveral, FL on a weekly and biweekly frequency. The results showed that grooming reduced fouling on all surfaces and was able to prevent fouling on the ablative copper and FR coatings when performed weekly. It was concluded that the grooming tool used for these tests was sufficient to remove biofilm and most hard fouling. However, when fouling pressure increased or when grooming was performed less frequently, insufficient forces were imparted by the brush to remove all of the established hard fouling organisms.     

Analysis of mechanical grooming at various frequencies on a large scale test panel coated with a fouling-release coating

A mechanical grooming test was performed on large scale steel test panels coated with a fouling-release (FR) coating (International Intersleek 900), at four different frequencies, during the high fouling season in Port Canaveral, Florida. Grooming at frequencies of three or two times per week was effective at removing heavy biofilm growth and significantly reduced macrofouling settlement. Mechanical grooming at lower frequencies of weekly or bi-weekly removed heavy biofilm growth but was much less effective at reducing macrofouling settlement. The results indicated that frequent mechanical grooming could reduce the fouling rating of ships coated with FR coatings. The reduction in the fouling rating of ships’ hulls by frequent grooming could offer significant reductions in drag, fuel consumption, and the emission of exhaust gases. Frequent grooming could also eliminate the need for hull cleaning and increase the time between dry docking which would reduce the operational costs for many vessel operators.     

Setal morphology of grooming appendages in the spider crab,Libinia dubia

In crustaceans, grooming behaviors decrease fouling by removing debris from the exoskeleton and body structures; these grooming behaviors improve respiration, sensory reception, movement, and reproduction. Setal morphologies of the following grooming appendages in the decapod crustacean spider crab Libinia dubia are examined including the first pereiopod (cheliped), first, second, and third maxillipeds (mouthparts), and first, second, and third epipods (internal extensions of the maxillipeds). The objective of this study was to describe setal morphologies of these grooming appendages and to elucidate possible functions and efficiencies of setal structures. Spider crabs are hypothesized to have elaborate setal morphologies, mainly for cleaning specialized decorating setae as well as for cleaning inside the gill chamber, which has a higher likelihood of becoming fouled compared to other decapods such as shrimps. Fourteen setal types are documented and included several varieties of serrate and pappose setae as well as simple setae, cuspidate setae, papposerrate setae, and canoe setae. Maxillipodal epipods in the gill chamber are free of fouling, suggesting the setation on the third maxilliped protopod has an efficient functional morphology in removing debris before water enters the gill chamber. Serrate setae may function for detangling and separating structures whereas pappose setae may function for fine detailed grooming. The cheliped is the only grooming appendage that can reach decorating setae and it contains only pappose setae; thus decorating setae is not likely groomed in a manner that would greatly decrease fouling. J. Morphol. 277:1045–1061, 2016. © 2016 Wiley Periodicals, Inc.     

The effects of grooming on a copper ablative coating: a six year study

More than 90% of US Navy Ships are coated with copper ablative paint. These ships may spend long periods of time pier-side, which makes them vulnerable to fouling. Hull grooming has been proposed as a means of maintaining the coatings in an operational condition. This study investigated the effect of grooming on a copper ablative coating exposed statically for six years. Grooming was performed weekly or monthly with controls left ungroomed. The fouling community was visually assessed, dry film thickness measurements were taken to monitor coating loss, and the copper leaching rates were measured. It was found that weekly and monthly groomed surfaces reduced fouling, and the ungroomed surfaces became fully fouled. Coating loss was similar for weekly, monthly and ungroomed surfaces. The results suggest that grooming is a viable method for maintaining copper ablative coatings in a fouling-free condition without adverse increases in the total copper output.     

Analysis of long-term mechanical grooming on large-scale test panels coated with an antifouling and a fouling-release coating

Long-term grooming tests were conducted on two large-scale test panels, one coated with a fluorosilicone fouling-release (FR) coating, and one coated with a copper based ablative antifouling (AF) coating. Mechanical grooming was performed weekly or bi-weekly using a hand operated, electrically powered, rotating brush tool. The results indicate that weekly grooming was effective at removing loose or heavy biofilm settlement from both coatings, but could not prevent the permanent establishment of low-profile tenacious biofilms. Weekly grooming was very effective at preventing macrofouling establishment on the AF coating. The effectiveness of weekly grooming at preventing macrofouling establishment on the FR coating varied seasonally. The results suggest that frequent mechanical grooming is a viable method to reduce the fouling rating of ships’ hulls with minimal impact to the coating. Frequent grooming could offer significant fuel savings while reducing hull cleaning frequencies and dry dock maintenance requirements.     

Gill-cleaning mechanisms of a dendrobranchiate shrimp, Rimapenaeus similis (Decapoda, penaeidae): description and experimental testing of function.

Observations on functional morphology and results from experiments demonstrate that setiferous epipods compose the major gill-cleaning mechanism in a penaeoid shrimp, Rimapenaeus similis. Epipods on the second maxillipeds and on pereopods 1-3 are equipped with long setae bearing an array of digitate scale setules. These multidenticulate setae reach to most gills and are jostled among them during limb movements. Experiments were performed in which epipods were removed from the gill chamber on one side (experimental) but not the other (control); treated animals were exposed to fouling in a recirculating water system for 2 weeks. Particulate fouling, measured by reduction in relative gill transparency, was significantly greater on experimental than control gills. The pereopodal exopods, not previously implicated in gill cleaning in any decapod, were similarly identified as important gill-cleaning structures. Equipped with long multidenticulate setae like those on the epipods, exopods sweep back and forth over the gill filaments just under the gill cover, areas not reached by the epipods. Exopod-ablation experiments were conducted that showed that exopods prevent particulate fouling on gill surfaces over which they sweep. The similarity in action of the passive gill-cleaning system of R. similis to that of crayfish (Bauer [1998] Invert Biol 117:29-143) suggests the hypothesis that the epipodal and exopodal cleaning setae of R. similis are ineffective against epibionts. The reduction in epipodal and exopodal cleaning systems that occurs in the Penaeoidea is hypothesized to be compensated for by increased development of gill-cleaning setae on the branchiostegite, scaphognathite, or other structures.     

Commensalism or mutualism: conditional outcomes in a branchiobdellid–crayfish symbiosis

A growing body of evidence suggests that the costs and benefits involved in cleaning interactions can vary over space and time depending on the environmental conditions. However, whether the same cleaners actually induce variable net outcomes in terms of host fitness remains unclear to date. Branchiobdellid annelids are generally regarded as commensals or rarely parasites of their freshwater crayfish hosts, but a recent study suggests that they may also function as cleaning organisms. Under natural conditions, crayfish can experience fouling of the exposed surfaces of their exoskeletons and their gills (e.g., epibiosis) by various epibionts and particles of organic debris, and branchiobdellids graze on these sources of fouling. Here, we examined the extent to which variation in fouling pressure in the environment alters the outcome of the interaction between branchiobdellids and their crayfish host Cambaroide similis. A series of manipulations were performed in artificial environments designed to simulate either high or low fouling pressure. We used crayfish growth rates and mortality as direct measurements of the net costs and benefits of cleaning. Branchiobdellids had no significant effect on crayfish growth or mortality when cultured under low fouling pressure. However, their presence had a significant positive impact on host growth rates when cultured under high fouling pressure. These results suggest that the relationship between crayfish and branchiobdellids can fluctuate between commensalism and mutualism depending mainly on the environmental fouling pressure. We hypothesize that the outcome of cleaning interactions may largely depend on the factors directly related to the need for cleaning, such as parasite loads or fouling pressure.     

Decapod crustacean chelipeds: an overview

The structure, growth, differentiation and function of crustacean chelipeds are reviewed. In many decapod crustaceans growth of chelae is isometric with allometry level reaching unity till the puberty moult. Afterwards the same trend continues in females, while in males there is a marked spurt in the level of allometry accompanied by a sudden increase in the relative size of chelae. Subsequently they are differentiated morphologically into crusher and cutter making them heterochelous and sexually dimorphic. Of the two, the major chela is used during agonistic encounters while the minor is used for prey capture and grooming. Various biotic and abiotic factors exert a negative effect on cheliped growth. The dimorphic growth pattern of chelae can be adversely affected by factors such as parasitic infection and substrate conditions. Display patterns of chelipeds have an important role in agonistic and aggressive interactions. Of the five pairs of pereiopods, the chelae are versatile organs of offence and defence which also make them the most vulnerable for autotomy. Regeneration of the autotomized chelipeds imposes an additional energy demand called “regeneration load” on the incumbent, altering energy allocation for somatic and/or reproductive processes. Partial withdrawal of chelae leading to incomplete exuviation is reported for the first time in the laboratory and field inMacrobrachiumspecies.     

Grooming behavior and morphology of the caridean shrimp Pandalus danae Stimpson (Decapoda: Natantia: Pandalidae)

Grooming or cleaning is a frequent behaviorial activity of the shrimp Pandalus danae . Setal brushes on thoracic limbs scrape and rub other appendages and general surfaces of the exoskeleton. Chelate limbs nip and pick at edges of crevices in the cephalothoracic region. Scanning electron microscopy reveals that the setae composing the grooming brushes are equipped with characteristic tooth- and scale-like setules which serve as the actual rasping devices. Antennules, antennae and pereopods are frequently preened by the third maxillipeds and first pereopods, while large areas of the exoskeleton are cleaned by the third pair of walking legs and the chelate limbs.
Shrimp with the general cleaning limbs ablated develop significantly greater infestations of the epizoic suctorian Ephelota than animals allowed to groom. Olfactory hairs on the antennules of shrimp deprived of the third maxillipeds become fouled with diatoms and debris while those on controls do not. Grooming behavior clearly prevents a build-up of settling organisms between molts and repeated cleaning of sensory sites is essential in maintaining contact with the environment.     

Detection of dairy fouling: Combining ultrasonic measurements and classification methods

Fouling and cleaning in heat exchangers are severe and costly (up to 0.3% of gross national product) issues in dairy and food processing. Therefore, reducing cleaning time and cost is urgently needed. In this study, two classification methods [artificial neural network (ANN) and support vector machine (SVM)] for detecting protein and mineral fouling presence and absence based on ultrasonic measurements were presented and compared. ANN is based on a multilayer perceptron feed forward neural network, whereas SVM is based on clustering between fouling and no fouling using a hyperplane. When both fouling types (1239 datasets) were combined, ANN showed an accuracy of 71.9% while SVM displayed an accuracy of 97.6%. Separate fouling detection of mineral/protein fouling by ANN/SVM was comparable: dependent on fouling type detection accuracies of 100% (protein fouling, ANN and SVM), and 98.2% (SVM), and 93.5% (ANN) for mineral fouling was reached. It was shown that it was possible to detect fouling presence and absence offline in a static setup using ultrasonic measurements in combination with a classification method. This study proved the applicability of combining classification methods and fouling measurements to take a step toward reducing cleaning costs and time.     

Towards an absolute scale for adhesion strength of ship hull microfouling

In-water ships’ hull cleaning enables significant fuel savings through removal of marine fouling from surfaces. However, cleaning may also shorten the lifetime of hull coatings, with a subsequent increase in the colonization and growth rate of fouling organisms. Deleterious effects of cleaning would be minimized by matching cleaning forces to the adhesion strength of the early stages of fouling, or microfouling. Calibrated waterjets are routinely used to compare different coatings in terms of the adhesion strength of microfouling. However, an absolute scale is lacking for translating such results into cleaning forces, which are of interest for the design and operation of hull cleaning devices. This paper discusses how such forces can be determined using computational fluid dynamics. Semi-empirical formulae are derived for forces under immersed waterjets, where the normal and tangential components of wall forces are given as functions of different flow parameters. Nozzle translation speed is identified as a parameter for future research, as this may affect cleaning efficacy.     

Head grooming behaviour in the praying mantis

Mantis head grooming is a rhythmic behaviour pattern involving co-ordinated movements of head and foreleg. The probability of grooming is influenced by releaser concentration, while the number of cycles/episode is influenced by concentration and amount of releaser. Within a grooming episode (usually 4 to 6 cycles) successive cycles are longer in duration; this is primarily caused by an increase in the actual head cleaning phase, although all three phases increase in duration. The phase cleaning the femur brush is most sensitive to feedback effects from releaser substances. It is concluded that head grooming is a programmed, i.e. centrally organized, movement pattern responsive to peripheral feedback. First approximations to the model-equations and model-hypotheses are presented.     

Ontogenetic shift in host tolerance controls initiation of a cleaning symbiosis

When the interests of mutualists are not perfectly aligned, control mechanisms that modulate interactions can maintain mutually beneficial outcomes and stabilize mutualisms over evolutionary time. However, the costs and benefits of symbiosis often change with ontogeny and whether control mechanisms are adjusted to reflect ontogenetic changes is largely unknown. We examined the recently described cleaning symbiosis between crayfish Cambarus chaugaensis and ectosymbiotic annelids (Xironodrilus appalachius) for evidence of ontogenetic changes in symbiont control. Xironodrilus appalachius provide a beneficial cleaning service to C. chaugaensis by removing epibiotic accumulations from the gills, but crayfish also incur costs via density‐dependent facultative parasitism of gill tissue. A series of laboratory experiments using crayfish from three size (age) – classes demonstrated that crayfish use grooming to limit cleaner density and grooming effects on cleaners varied with crayfish age. Small crayfish quickly removed essentially all of their cleaners. Intermediate crayfish removed most of their cleaners, but some cleaners persisted at a location apparently inaccessible to grooming and far from the gill chamber. Large crayfish removed a smaller proportion of cleaners and cleaners were allowed access to the gill chamber, thus initiating the cleaning symbiosis. Cleaner removal was not dependent on cleaner density, suggesting that crayfish do not regulate cleaners to a specific density. Experimental results were corroborated by patterns observed during a field survey. We argue decreased cleaner removal and relaxed control of cleaner attachment sites corresponds to ontogenetic changes in the costs and benefits of symbiosis. This study integrates two major theoretical perspectives from ecological literature; control mechanisms and ontogenetic shifts, and illustrates how changes in control mechanisms with ontogeny may favor life‐long positive outcomes of symbiosis. Ontogenetic shifts in the costs and benefits of symbiosis may be common; therefore future theoretical and empirical studies of symbioses should incorporate both perspectives.     

Economic impact of biofouling on a naval surface ship

In the present study, the overall economic impact of hull fouling on a mid-sized naval surface ship (Arleigh Burke-class destroyer DDG-51) has been analyzed. A range of costs associated with hull fouling was examined, including expenditures for fuel, hull coatings, hull coating application and removal, and hull cleaning. The results indicate that the primary cost associated with fouling is due to increased fuel consumption attributable to increased frictional drag. The costs related to hull cleaning and painting are much lower than the fuel costs. The overall cost associated with hull fouling for the Navy's present coating, cleaning, and fouling level is estimated to be $56M per year for the entire DDG-51 class or $1B over 15 years. The results of this study provide guidance as to the amount of money that can be reasonably spent for research, development, acquisition, and implementation of new technologies or management strategies to combat hull fouling.     

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.     

Ship hull in-water cleaning and its effects on fouling-control coatings

Abstract

Today, ship hull fouling is managed through fouling-control coatings, complemented with in-water cleaning. During cleaning, coating damage and wear must be avoided, for maximum coating lifetime and reduced antifoulant release. When possible, cleaning should target early stages of fouling, using minimal forces. However, such forces, and their effects on coatings, have not yet been fully quantified. In this one-year study, minimal cleaning forces were determined using a newly-designed immersed waterjet. The results show that bi-monthly/monthly cleaning, with maximum wall shear stress up to ～1.3?kPa and jet stagnation pressure ～0.17?MPa, did not appear to cause damage or wear on either the biocidal antifouling (AF) or the biocide-free foul-release (FR) coatings. The AF coating required bi-monthly cleanings to keep fouling to incipient slime (time-averaged results), while the FR coating had a similar fouling level even without cleaning. The reported forces may be used in matching cleaning parameters to the adhesion strength of the early stages of fouling.     

Recent book

In the present study, the overall economic impact of hull fouling on a mid-sized naval surface ship (Arleigh Burke-class destroyer DDG-51) has been analyzed. A range of costs associated with hull fouling was examined, including expenditures for fuel, hull coatings, hull coating application and removal, and hull cleaning. The results indicate that the primary cost associated with fouling is due to increased fuel consumption attributable to increased frictional drag. The costs related to hull cleaning and painting are much lower than the fuel costs. The overall cost associated with hull fouling for the Navy's present coating, cleaning, and fouling level is estimated to be $56M per year for the entire DDG-51 class or $1B over 15 years. The results of this study provide guidance as to the amount of money that can be reasonably spent for research, development, acquisition, and implementation of new technologies or management strategies to combat hull fouling.     

Selectivity in vector management: an investigation of the effectiveness of measures used to prevent transport of non-indigenous species

Measures taken to control the spread of non-indigenous species by human vectors may act selectively by providing effective protection against some (but not all) species. Toxic antifouling paints are used by boat owners to prevent the development of fouling assemblages on the hulls of their boats, which reduce vessel speed and maneuverability. By reducing fouling, these paints also prevent transport of non-indigenous species. Using experimental surfaces mimicking boat hulls, we evaluated the effectiveness and selectivity of (1) antifouling paints, and (2) manual, in-water hull cleaning for preventing the transport of marine sessile invertebrates by recreational vessels. Different types of antifouling paints provided effective protection only against barnacles and bivalves. Other fouling taxa occurred on experimental surfaces after a period of only 2 months. Manual hull cleaning did not remove fouling completely, and even enhanced the risk of subsequent recruitment by some fouling organisms. Up to six times more individuals and colonies recruited to boat surfaces from which the existing fouling organisms had been removed manually than to surfaces that had been sterilized or contained intact fouling assemblages. Bivalves, colonial and solitary ascidians, encrusting bryozoans, hydroids, tubiculous polychaetes, and sponges consistently recruited in greatest abundance to manually cleaned surfaces. Individual taxa responded in complex, but predictable ways to the biogenic cues left by manual cleaning, so that different suites of organisms colonized surfaces that had originally contained fouling assemblages of local or non-local origin. Our study shows that widely adopted measures to control the spread of non-indigenous species by human vectors are often highly selective and, while effective for some taxa, do not prevent the transport of others.