title for limpet section of the Odyssey
  Physiological topics relating to limpets include sensory, gas exchange, osmotic regulation, internal defense, and digestion are dealt with in this section.
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  Sensory organs of larval limpets include apical ciliary tufts. Those of adult limpets include eyes, cephalic tentacles, and mantle tentacles. These last extend outwards from the mantle edge and are in intimate contact with the substratum. In fact, as the head and cephalic tentacles barely peek out from the shell these tentacles may provide much of the chemotactile information used by a limpet for locomotory navigation, finding food, and avoiding predators. Having said this, not a lot of information is available on west-coast species.
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Research study 0

drawing of eyespot of limpet Patellaphotograph of limpets Lottia limatulaSo-called eyes of limpets are shallow pits at the base of each cephalic tentacle lined by sensory cells containing pigment granules (see drawing). The eyespots are light-sensitive only, with no visual resolution. A study at Hopkins Marine Station, California on Lottia limatula reveals that the eyes are sensitive not only to white light, but also differentially to blue, green, and red wavelengths. Responses to light stimuli in all species are negatively phototactic, involving backing and sideways movements, culminating in 180o reversal. As animals with their eyes experimentally removed will still respond to high-intensity white and blue light, the author suggests the presence of other, yet undescribed, light-receptive organs, perhaps in the mantle tentacles. Ross 1968 Veliger (Suppl.): 11: 25; drawing of eye-spot of limpet Patella courtesy J. Heller 2015 Sea snails Springer, Inc; photograph courtesy James Watanabe, Hopkins Marine Station, California SEANET

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Research study 1

photograph of juvenile limpet Lottia personaphotographs of shell of limpet Lottia persona taken with illumination from above and belowThe high-level limpet Lottia persona hides in shady cracks and overhangs during the day, and emerges at dusk to feed. One supposes that it uses its light-sensitive eyespots to assess environmental light levels, but is this done from light entering from below the shell edge or through the shell? Researchers at San Francisco State University note that the white spots at the anterior end of the shell are translucent and allow light to enter (see photographs on Right). Spots at the back are not translucent because opaqueshell material is deposited overtop of them. To answer the question posed above, the researchers compare behaviour to light of limpets wearing tight-fitting shell-shaped opaque plastic cowlings, with ones with similar cowls but with the anterior portions removed. A control treatment uses normal, cowl-less animals. Tests involve exposing members of each treatment group in a darkened trough to illumination from a light located 15cm in front, with turning away from the light by >90o indicating a positive response. Light intensity is 40 foot-candles (12.6 lumens), selected from field readings taken under different daytime weather conditions. Results show that control and partially cowled individuals exhibit mean response times of 73 and 81sec, while fully cowled individuals respond only after 121sec. A separate field test using a tarpaulin to shade feeding animals at night provides corroborative evidence. When the tarpaulin is removed several hours after dawn, the animals are still feeding, while adjacent unshaded animals have long since sought out shelter. The authors do not discuss why light coming in from under the front of the shell is not sufficient stimulus for the limpets; however, perhaps when feeding the head is pressed forward and blocks this source of illumination. Lindberg et al. 1974 The Veliger 17 (4): 383; illuminated shell photographs courtesy the authors.

NOTE the researchers use only 23 individuals in the tests, allowing a day’s rest between tests. All are cowled at the beginning, but 5 cowls fall off during a 24h “cowl-acclimation” period. Apparently, all 18 cowled individuals are tested, then re-tested after their cowls are cut away at the front. The researchers do not mention how many repeats there may have been or how many failures, how 10 cowl-less control animals are chosen from the 5 available, how many individuals are used repeatedly and in what order, or the impact on their results of this rather jumbled protocol. A better experimental design would have been to start with as many animals as needed for a single test on each for each treatment or, alternatively, to have used a repeated-measures protocol where each individual is tested cowl-less (control), cowled, and then partially cowled. The statistical test used requires independent sampling, which does not happen

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Research study 2

photograph of limpet Lottia scutum showing location of tentacles along the mantle edge
A study on Lottia scutum at Bodega Marine Laboratory, California explores the possible sensory functions of the many tentacles along the mantle edge.  The functions likely include food and predator sensing.  Each tentacle is crowned with a dense cap of stiff cilia and additional tufts are spread along the tentacle length.  Two types of sensory cells are evident on the tentacles, but the author is unable to assign functions to each based solely on ultrastructure.  In addition to the tentacle sensory cells, there are abundant photoreceptors on the mantle margin, and mechanoreceptors sensitive to touch and water currents.  Phillips 1977 Veliger 19: 266; Phillips 1979 Tissue & Cell 11: 623.




Upside-down Lottia scutum showing foot, head, mouth, tentacles, and
mantle edge. The foot is just beginning to curl inwards as the animal
senses that it is not the right way up. The curly stuff at upper Left is
fecal matter, issuing from the anus located to the Right of the head

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Research study 3
  photographs of veliger larvae of a plate limpet Lottia scutum showing the apical tuftsVeliger larvae of limpets have an apical sensory organ that is described in detail by a researcher at the University of Victoria, British Columbia for plate limpets Lottia scutum. The organ comprises just a few cells that together produce 3 ciliary tufts and are linked to a neural (apical) ganglion. Most or all molluscan larvae have such apical tufts, but their precise function is still uncertain. One of the more popular ideas is that it provides chemosensory information relating to selection of a suitable substratum on which the larva will settle and metamorphose. Page 2002 Biol Bull 202: 6; photographs courtesy the author.

Gas exchange

This section includes studies on limpets (Lottia spp.), keyhole limpets (Diadora aspera), and pulmonate "limpets" (Trimusculus reticulatus). The last superficially resembles a limpet and sometimes is called a "false limpet", but actually it is less closely related to limpets than to air-breathing land snails.
Research study 1

photograph of limpet Lottia pelta to show the direction of water flow through the mantle cavitydrawings of owl limpt Lottia gigantea with shell removed to show position of ctenidium and the water flow through the mantle cavityWhereas keyhole limpets have paired ctenidia, all “true” limpets (F. Acmaeidae) have a single ctenidium (the right one is lost in evolution).  The pattern of water flow for gas exchange for most west-coast species, including owl limpets Lottia gigantea, is into the mantle cavity from the left side, through the ctenidium, and out the right side (see drawing above Left, and photo). As the water flow exits the mantle cavity it receives discharge from the nephridiopore (urine) and anus. 

There are varying amounts of secondary flow through the pallial groove around the foot.  In most species, these tend to be cleansing flows rather than gas-exchanging ones.  drawing of limpet's pallial groove to show location of pallial gillsHowever, in L. gigantea there are many secondary, or pallial, gills arranged lappet-like in the pallial groove (see drawing lower Left). These are irrigated by weak water currents driven by cilia up and through the pallial gills (indicated by small arrows in the drawing).  As the shell is seldom clamped firmly down during low-tide periods, air spaces are likely present for aerial gas exchange.  The cilia may circulate a water film over the pallial gills and associated mantle surface.  The author notes that this is the first report of water currents for gas exchange in owl limpets.  Abbott 1956 The Nautilus 69: 79.

Research study 1.1

drawing from below of a pulmonate limpet Trimusculus reticulatusObservations on pulmonate “limpets” Trimusculus reticulatus by a researcher at Hopkins Marine Station, Pacific Grove, California suggest that gas exchange may be possible in both air and water.  The author describes a typical pulmonate pneumostome on the right side of the head that opens to allow air to circulate through the spacious mantle cavity (pallial groove; see drawing).  This cavity is lined by a thin epithelium, unciliated except for the channel leading to the exterior via the pneumostome.  An ability to repire both in air and water is suggested by the author’s witnessing the pneumostome opening widely to admit water in an immersed individual, and with the water visibly moving along the passage from pneumostome to mantle cavity.  However, the details of this behaviour are rather sketchy, and no mention is made of survival times of individuals continually immersed (see also Research Study 3.1 below).  Yonge 1958 J Malacol Soc Lond 33: 1.

NOTE  viewed from below with the animal on a glass slide

NOTE  this entire topic of gas exchange and survival in water would make a good research project for someone

Research study 2

drawings of limpets Lottia spp. to show ciliary currents through pallial groove and mantle cavityLottia paleacea lives exclusively on fronds of surfgrass Phyllospadix spp. in high-energy surf conditions.  Perhaps for this reason its shell fits tightly to the frond.  A notch is present on the right-hand side to accommodate water flow for gas exhange. Most other west-coast species have water-current patterns for gas exchange similar to that shown above for L. gigantea (see drawing). Lottia pelta differs from other species in not having cleansing currents in the pallial groove. Yonge 1962 Veliger 4: 119.

Research study 2.1
  drawing of limpet Lottia sp. as seen from below showing water flow patternShould you wish to observe water flow through the mantle cavity of a limpet Lottia sp. with the subject in normal upright posture, a handy method using an inverted dissecting microscope is described by a researcher at Pacific Marine Station, California. The experimenter views the limpet in its dish of seawater from below, with injections of carmine dye being used to monitor water flow. The system can be used in either field or laboratory settings. Water flow is from left to right, bracketing the single ctenidium and splitting as it moves posteriorad along the right side of the mantle cavity (see drawing). Along the way the flow picks up urinary excretions from the nephridiopores, fecal matter from the anus and, in season, gametes from the right nephridiopore. Fankboner 1966/67 Veliger 9 (2): 251.
Research study 3

photograph of limpet Lottia digitalis

In Pacific Grove, California limpets Lottia digalis and L. scabra live sympatrically, but with the former species favouring more vertical rock surfaces and latter species inhabiting horizontal surfaces.  Measurements of rates of oxygen uptake of the 2 species at Hopkins Marine Station, California show that rates are higher in both when submerged than when air-exposed. The difference between the 2 conditions is most exaggerated for L. scabra than for L. digitalis.  Baldwin 1968 Veliger 11 (Suppl.): 79.

NOTE the graph shows cumulative oxygen consumption over a 2-h period

graph comparing oxygen uptake in limpets Lottia digitalis and L. scabra in and out of water
photograph of limpet Lottia digitalis
Research study 3.1

drawing of limpet with parts of circulatory system imposedFrom the foregoing studies it seems like gas exchange occurs only via the ctenidium in limpets, but this is not the case. In fact, any thin, diffusible surface with hemolymph on one side and oxygen-bearing seawater on the other side may function for gas exchange. This is investigated by a researcher at Hopkins Marine Station for limpets Lottia digitalis, L. pelta, and L. scutum, representing high-, medium-, and low-level species, respectively. To determine which surfaces function in gas exchange, the researcher injects colloidal carbon or vital (non-toxic) dye solutions into the hemolymph and assays for visual presence of the stain microscopically through the thin epithelium. If the injected fluid is dilute enough, flow direction of the hemolymph can also be observed. Results show that flow is partly in vessels and partly within large open sinuses, as in the foot. From the heart, efferent (“away”) vessels carry hemolymph anteriorly to buccal and head areas, and posteriorly to the visceral cavity, and thence to the ctenidium. From the ctenidium the flows splits into a return pathway to the heart, and one to the mantle and to the circumpallial (“around the mantle”) vessel. It is this last that is of most interest here because it branches into a large plexus of vessels that by their area and proximity to the seawater flowing through the mantle cavity, likely act as sites of auxiliary gas exchange. This is supported by the fact that from the large circumpallial vessel the hemolymph enters the anterior afferent (“towards”) vessel that leads directly to the heart. Field observations of limpets in air indicate that the ctenidium is largely withdrawn, while the mantle vessels are swollen and gorged with hemolymph. Conversely, in water the ctenidium is extended and ciliary currents (stained with carmine) are seen to move counter to the known ctenidial hemolymph flow. Ctenidial length in the high-intertidal L. digitalis is shorter than in the mid/low intertidal-dwelling L. pelta and L. scutum. The author concludes that ctenidial function is more important when in water, while the mantle comes into play more when in air. Kingston 1968 Veliger 11 (suppl.): 73; drawing of limpet (without vessels) courtesy Peter Fankboner, Simon Fraser University.

NOTE in areas of fine capillary networks such as ctenidial and circumpallial regions where the carbon particles are too large to transit, vital dyes such as carmine are used

Research study 3.2

schematic showing location of air bubbles in subtidal cavesA researcher at Harvey Mudd College, Claremont, California describes an unusual habitat for air-breathing intertidal pulmonates Trimusculus reticulatus within air bubbles caught on the underside of a subtidal ledge.  The bubbles appear to be naturally formed from air suspended by wave action at high tide.  The situation is fine for subtidal gas exchange using a lung (mantle cavity), but comes with a cost.  Trimusculus is a suspension-feeder, and so must wait for the bubble to dissipate in order to feed.  However, given the risk of not being able to find new bubbles to survive, one wonders if the “habitat” might be happenstance and not one that can be permanently occupied.  The researcher assesses the “refill capacity” of the system by emptying air pockets and checking rate of regeneration, but a regularised protocol of checking is stymied by rough surf conditions.  On one occasion 9 SCUBA divers pass close to the ledge either to or from their dive site with no apparent effect on air-bubble size or number.  The study is short but interesting, and leaves the reader wanting more.  One immediate question is the extent to which the snail can utilise dissolved oxygen in water as well as gaseous oxygen via its lung. Haddock photograph of pulmonate "limpet" Trimusculus reticulatus1989 The Veliger 32: 403. Photograph courtesy Gary McDonald, Long Marine Laboratory, Santa Cruz & CALPHOTOS.

NOTE  the author uses gas-chromatography to test whether the source of the air pockets comes from SCUBA activity, but the results are not conclusive.  The bubbles contain <0.5% CO2, while air contains about 0.04% and human exhalation about 3% 

Pulmonate "limpet" Trimusculus
encrusted with
tubeworms 2.5X

Research study 4

photograph of keyhole limpt Diodora asperaWater flow for gas exchange in keyhole limpets Diodora aspera is also driven by beating of cilia lining the mantle cavity.  The pattern of flow is in over the head and sensory tentacles, over the paired ctenidia for gas exchange, upwards past the kidney and reproductive openings, then past the anus and, finally, out the hole in top.  This pattern ensures that waste products are directed away from the limpet without contaminating the head and gills.  The pattern described here supports a long-held idea that sanitation is the primary factor involved in evolution of mantle-cavity design and water flow in molluscs. The hole in the shell of Diodora also tends to operate passively; that is, water drawings of keyhole limpets to show water currents through mantle cavity with hole open and pluggesflowing over it causes water to be “pulled” out of the mantle cavity, thus augmenting the gas-exhange flow described above. 

Interestingly, if the hole in Diodora is blocked either naturally or experimentally with a plug of clay there is no observable deleterious effect on the animal, giving rise to the suggestion that, rather than the hole being primarily for sanitation (allowing feces and urine to be released without contaminating the head and gills), it may be equally important in inducing passive flow.  Voltzow & Collin 1995 Invert Zool 114: 145.

  there is actually no shortage of ideas relating to the function of the hole in Diodora’s shellThe fact that a keyhole limpet appears to maintain good health with its hole blocked suggests a function unrelated to sanitation or gas exchange - for example, reproduction.  Perhaps the hole in the shell increases fertilisation success by releasing the gametes well above the substratum surface where they would float for a longer time and have more chance of meeting gametes of the opposite sex

Research study 5

diagrammatic representation of design elements of the mantle cavity of a keyhole limpet Diodora asperadrawing showing flow pattern through the mantle cavity of a keyhole limpet Diodora aspera

Water flow for gas exchange in a keyhole limpet Diodora aspera enters the mantle cavity on either side of the head, flows upwards past and through the ctenidia, and exits via the hole at the top of the shell. On its way out it picks up urinary and fecal wastes (see diagram on Right). Theoretically, the flow can be modeled on the Principle of Continuity that describes flow through pipes.  The Principle states that the volume-flow rate, or the product of the cross-sectional area and velocity, remains constant along the length of the pipe (see diagrammatic representation of the mantle cavity of Diodora on Left). Studies at Friday Harbor Laboratories, Washington using dyes to visualise flow patterns, and transport of neutrally buoyant particles to determine flow rates show, indeed, that water flow through the mantle cavity does accord with the Principle.The author comments that this information allows flow rates along any part of the flow path to be predicted.  Voltzow 2004 Am Malacol Bull 18: 155.

NOTE  the author also includes the tulip shell Fasciolaria hunteria in the study, a species not found on the west coast of North America

NOTE  flow volume is approximately 40 mm3 . sec-1 for an individual of 14g live mass

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Research study 6

schematic endoscopic view of the ctenidial structure within the mantle cavity of a keyhole limpet Diodora asperaIn a later study also at Friday Harbor Laboratories, Washington the same author employs an endoscope inserted into the ventilatory holes of keyhole limpets Diodora aspera to gain novel views of the ctenidia in action. Unfortunately, the field of view is small and the ctenidia mostly fill the mantle cavity. One feature not seen in dissections, however, are the large and inflated afferent branchial vessels. These dorsal vessels transport deoxygenated hemolymph through the ctenidial filaments to the ventral receiving efferent branchial vessels, and thence to the heart. The oxygenated hemolymph is then circulated to the rest of the body. In that the hemolymph flow through the ctenidia is generally dorsal to ventral and water flow through the mantle cavity ventral to dorsal, there is a counterflow exchange taking place, discussed by the author. Small (25um dia) polystyrene beads introduced into the mantle cavity in the incurrent seawater flow are observed to be bound up in mucous strings and moved away by ciliary action. Introduction of milk or dye solutions create streaklines that maintain their integrity as they are moved through the filaments, and out of the apical shell opening and beyond (see Research study 5 above). Interestingly and probably not surprisingly, numerous small crustaceans swim freely through the mantle cavity and ctenidial leaflets. Voltzow 2015 J Morph 276: 787.

NOTE also included in the study are similar views into the mantle chambers of red abalones Haliotis rufescens done at the Steinhart Aquarium, San Francisco, not dealt with here


Osmotic regulation

Research study 1

photograph of cluster of limpets Lottia scutum in a tidepool
The limpet Lottia scutum tends to favour tidepools, where rainfall may create fluctuating salinity conditions.  Studies at the University of British Columbia show that the species is, in general, an osmoconformer. Hemolymph and urine concentrations of sodium, chloride, calcium, and magnesium are the same as in experimental  seawater media over a range of test salinities from 50 to 125%. Webber & Dehnel 1968 J Exp Zool 168: 327; Webber & Dehnel 1968 Comp Biochem Physiol 25: 49.

NOTE  where 100% = 32‰

Research study 2

photograph of limpet Lottia scutum upside-down, but not swelling because it is not immersed.  Note the feces accumulating from the anus on the right-hand sideLarge volume changes, up to 100% of the volume of soft tissues, are observed in limpets Lottia scutum when they are turned upside-down under water.  Experiments on specimens collected at Jordan River, British Columbia and Monterey, California using inulin and other dye markers confirm that the volume increase occurs by bulk movement of seawater into hemocoelic spaces, perhaps via the gut.  The function, if any, of the volume uptake is not known.  Webber 1970 Veliger 12: 417.





Lottia scutum upside-down, but not swelling because it is not immersed.
Note the feces accumulating from the anus on the right-hand side 2.2X


Internal defense

Research study 1

A paper by researchers at Occidental College, California on hemocyte structure and function in giant keyhole limpets Megathura crenulata is somewhat outside the “whole-animal biology” scope of interest in the ODYSSEY, but some readers may be unaware that most or perhaps all marine invertebrates have internal defense systems. These consist of phagocytic cellular elements such as hemocytes, and humoral elements such as agglutinins. The hemocyte cells in Megathura (and also Aplysia) are of a single type and are carried thoughout the body in circulating hemolymph fluid. The cells are nucleated and in Megathura are ovoid in shape (about 8µm dia). They are phagocytic and readily engulf “non-self” particles of vital dyes and even larger sized yeast cells. The hemocytes contain abundant lysozymes, enzymes specialised for digesting bacterial cell walls. The pattern of defense against invading microorganisms involves an initial recognition by special soluble proteins, opsonins or agglutinins that bind to and so identify “non-self” particles. The wandering hemocytes respond to the identified particles by phagocytosing and digesting them. Undigested material may be eliminated by the hemocytes discharging their contents through the external epithelium or sometimes even by squeezing themselves through the outside tissues in a kind of “suicide” behaviour. Martin et al. 2007 J Moll Stud 73: 355; photographs courtesy the authors.photographs of hemocytes of a giant limpet Megathura crenulata

NOTE the sea hare Aplysia californica is also included in the study, and has hemocytes of similar structure and function to those of Megathura

NOTE throughout their description the authors carelessly describe the molluscan hemolyph as “blood”, that contains hemocytes within “plasma”. Neither term is appropriate for molluscs with open circulatory systems, and the terms should not have been used in the Journal of Molluscan Studies whose reviewers and editors know better

Left: isolated hemocyte from the giant limpet Megathura crenulata
Right: 10min after being placed onto a glass microscope slide the cells flatten to larger diameter, and extend engulfing and locomotory processes known as filopodia and lamellipodia



Research study 1

photo/schematic of the gut of a keyhole limpet Megathura crenulata showing regions of enzymatic productionThe digestive tract in limpets, as in other herbivorous animals, is relatively long, reflecting the general indigestibility of algal foodstuffs consumed. In the giant keyhold limpet Megathura crenulata, in additon to breakdown of food by the radula there is a pair of sharp jaws in the anterior esophagus for macerating larger food bits (absent from lottiid-type limpets), a feature underscoring the broad dietary range of fissurellid limpets. All subsequent digestion in the gut is done chemically through enzymatic action. A detailed study1 by researchers at Occidental College, California of digestion in Megathura reveals that all parts of the gut are involved, not just the digestive gland as one might have thought. Note in the photo/schematic that the gut is about 3 times longer than the shell and can be divided into 7 morphological regions. The tissues of these 7 plus 3 additional areas, representing subdivisions of the middle- and posterior-esophagal regions, are sampled for 19 enzymes. Results show that proteases are produced mainly in the esophageal and crystalline-style2 regions, and amylases, celllulases, and lysozymes3 in the crystalline style. Lipases are mainly produced in the digestive gland and crystalline style regions. To a limited extent proteases, lysozymes, and lipases are also secreted from tissues of the intestinal loop, perhaps a last pulse of “digestivity” prior to transit through the intestine. Also, not shown very well in the schematic, the salivary glands contribute enzymes in the anterior esophageal region. Cellulases are not strongly represented in Megathura and, as thought for other invertebrate herbivores, cellulose digestion may primarily be done by gut bacteria. The rich production of amylase enzymes by the crystalline style reflects the strong carbohydratae component of Megathura's diet. Contrary to the function suggested by its name, the digestive gland itself produces only small amounts of enzymes. However, it connects to and receives a rich enzymatic slurry from the stomach, provided by the crystalline style that sits in a pouch extending off the stomach. The digestive gland is the primary site of digestion and absorption in Megathura as in all gastropods. The stomach sits juxtaposed to the digestive gland and is itself lined by chitin. It thus acts mainly as a sorting area with conduits to the digestive gland and then, via separate counter-flow ciliary ducting, enabling return of material from the digestive gland to the intestine. As already noted, some enzymes are produced in the “intestinal loop”, indicating that the intestine actually plays a role in digestion and does not merely function in compaction of indigestible materials. Although primarily considered a herbivore, the present study shows that Megathura is capable of digesting a broad spectrum of organic materials (e.g., colonial tunicates are a favoured food, as well as other animal matter). Martin et al. 2011 Comp Biochem Physiol A 160: 365.

NOTE1 the main motivation for the study appears to be to learn about Megathura’s nutrition with the aim of culturing it for pharmaceutical purposes. Its blood pigment hemocyanin apparently has useful application in treating certain cancers and immunological conditions

NOTE2 we are more familiar with crystalline styles in bivalves. Such organs are absent in abalones and lottiid limpets, just to name some familiar gastropods, and their presence in fissurellids may simply underscore the wide array of foodstuffs consumed by them (e.g., colonial tunicates rank high on Megathura’s menu of preferred foods). The “crystalline style” area in the schematic actually combines both crystalline-style and style-sac values that are given separately in the authors’ original paper

NOTE3 lysozymes in vertebrates function to dissociate bacterial cell walls, suggesting that bacteria may be used as a food source by Megathura. While mentioning this in their discussion, the authors basically gloss over the potential contribution of gut bacteria in keyhole limpets and other herbivorous marine invertebrates in producing nutrients for their hosts (not just in being eaten by their hosts). This whole topic needs to be addressed