Search

SynopsisSpines are ubiquitous in both plants and animals, and while most spines were likely originally used for defense, over time many have been modified in a variety of ways. Here we take an integrative approach to review the form, function, and evolution of spines as a defensive strategy in order to make new connections between physical mechanisms and functional behavior. While this review focuses on spines in mammals, we reference and draw ideas from the literature on spines in other taxa, including plants. We begin by exploring the biomechanics of defensive spines, their varied functions, and nondefensive modifications. We pay particular attention to the mechanics involved in passive puncture and the ways organisms have overcome limitations associated with the low energy input. We then focus on the ecological, physiological, and behavioral factors that promote the evolution of spiny defenses, including predator- and habitat-mediated hypotheses. While there is considerable evidence to support both, studies have generally found that (1) defensive spines are usually effective against one class of attacker (e.g., larger predators) but ineffective against or even facilitate predation by others and (2) species that are more visible or exposed to predators are under much stronger selection to evolve defensive spines or some other robust defense. What type of defensive morphology that evolves, however, is less predictable and probably strongly dependent on both the dominant source of predation and the habitat structure of the organism (e.g., arboreal, terrestrial, and fossorial). We then explore traits that often are correlated with defensive spines and armor, potentially forming armor syndromes, suites of traits that evolve together with body armor in a correlated fashion. In mammals, these include aposematic warning coloration, locomotion style, diet, metabolic rate, and relative brain size. Finally, we encourage integration of mechanistic, behavioral, and evolutionary studies of defensive spines and suggest future avenues of research in the biomechanics, evolution, and behavior of spines and spiny organisms.

Synopsis Bull kelp (Nereocystis luetkeana), the only canopy-forming kelp in the Salish Sea, provides primary production in the nearshore subtidal environment and serves as an important habitat for economically and ecologically important species. An annual species, each year juvenile bull kelp sporophytes must grow from the hydrodynamically more benign benthos to the water column, where they experience substantial drag at the surface. Because of the differences in morphology and ecology across life stages, and the fact that previous work has focused mainly on adult bull kelp, we tested whether morphology and structural properties change with stipe length, investigating scaling of both juvenile (stipe length 40 cm) kelp, and testing how juvenile stipes fail. Juvenile bull kelp grow proportionally (isometric growth) when young, but lengthen more quickly than would be predicted by bulb size (negative allometry) at maturity. Based on our data, the predicted breakpoint between isometric and allometric growth occurred at about 33 cm, likely approximately one to two weeks of growth. Cross-sectional area of the stipe, force to failure, work to failure, and stiffness (Young's modulus) all grow more slowly than would be predicted based on length, while maximum stress and toughness increase more quickly than predicted. There is no change in extensibility over the size range we tested, suggesting that this material property does not change with stipe length. The differences in biomechanics between juvenile and adult kelp are likely a response to the varied hydrodynamic environments experienced during the annual life cycle, which highlights the importance of studying organisms across life stages.

Synopsis Teeth lie at the interface between an animal and its environment and, with some exceptions, act as a major component of resource procurement through food acquisition and processing. Therefore, the shape of a tooth is closely tied to the type of food being eaten. This tight relationship is of use to biologists describing the natural history of species and given the high instance of tooth preservation in the fossil record, is especially useful for paleontologists. However, correlating gross tooth morphology to diet is only part of the story, and much more can be learned through the study of dental biomechanics. We can explore the mechanics of how teeth work, how different shapes evolved, and the underlying forces that constrain tooth shape. This review aims to provide an overview of the research on dental biomechanics, in both mammalian and non-mammalian teeth, and to synthesize two main approaches to dental biomechanics to develop an integrative framework for classifying and evaluating dental functional morphology. This framework relates food material properties to the dynamics of food processing, in particular how teeth transfer energy to food items, and how these mechanical considerations may have shaped the evolution of tooth morphology. We also review advances in technology and new techniques that have allowed more in-depth studies of tooth form and function.

The skin and blubber of marine mammals provides protection from the surrounding environment, whether that be temperature, microbes, or direct mechanical impacts. To understand the ability of harbor seals' (Phoca vitulina) skin and blubber to resist blunt force trauma, we tested the material properties of these tissues. We quantified two mechanical properties of the tissue: tensile strength and tensile stiffness, at two test speeds, three sample orientations, and two age groups. We found significant differences in material properties between test speeds, orientation, and age of the animal, but did not find a large difference with orientation. From this analysis, we conclude that harbor seal skin and blubber should be modeled as an isotropic non-linear elastic material with strain rate dependence. Moreover, we were interested in the effects of freezing on the biomechanical properties. The material was tested fresh and after being frozen for four months. Frozen data revealed an increase in stiffness and strength for the skin (epidermis and dermis), but did not show a conclusive trend in the blubber material properties. While the availability of frozen marine mammal tissue is greater than that of fresh material, frozen tissue of harbor seals, especially the skin, cannot serve as an accurate replacement for testing of fresh material.

Placodontia were a group of marine reptiles that lived in shallow nearshore environments during the Triassic. Based on tooth morphology it has been inferred that they were durophagous, but tooth morphology differs among species: placodontoid placodonts have teeth described as hemispherical, and the teeth of more highly nested taxa within the cyamodontoid placodonts have been described as flat. In contrast, the sister taxon to the placodonts, Palatodonta bleekeri, like many other marine reptiles, has tall pointed teeth for eating soft-bodied prey. The goals of this paper are to quantify these different tooth morphologies and compare tooth shape among taxa and with a functionally “optimal” tooth. To quantify tooth morphology we measured the radius of curvature (RoC) of the occlusal surface by fitting spheres to 3D surface scans or computed microtomographic scans. Large RoCs correspond to flatter teeth, while teeth with smaller RoCs are pointier; positive RoCs have convex occlusal surfaces, and a negative RoC indicates that the occlusal surface of the tooth is concave. We found the placodontoid taxa have teeth with smaller RoCs than more highly nested taxa, and palatine teeth tend to be flatter and closer to the optimal morphology than maxillary teeth. Within one well-nested clade, the placochelyids, the rearmost palatine teeth have a more complex morphology than the predicted optimal tooth, with an overall concave occlusal surface with a small, medial cusp. These findings are in keeping with the hypothesis that placodonts were specialized durophagous predators with teeth modified to break hard prey items while resisting tooth failure.

Dental functional morphology, as a field, represents a confluence of materials science and biology. Modern methods in materials testing have been influential in driving the understanding of dental tissues and tooth functionality. Here we present a review of dental enamel, the outermost tissue of teeth. Enamel is the hardest biological tissue and exhibits remarkable resilience even when faced with a variety of mechanical threats. In the light of recent work, we progress the argument that the risk of mechanical degradation across multiple scales exhibits a strong and continued selection pressure on structural organization of enamel. The hierarchical nature of enamel structure presents a range of scale-dependent toughening mechanisms and provides a means by which natural selection can drive the specialization of this tissue from nanoscale reorganization to whole tooth morphology. There has been much learnt about the biomechanics of enamel recently, yet our understanding of the taxonomic diversity of this tissue is still lacking and may form an interesting avenue for future research.

An organism’s ability to control the timing and direction of energy flow both within its body and out to the surrounding environment is vital to maintaining proper function. When physically interacting with an external target, the mechanical energy applied by the organism can be transferred to the target as several types of output energy, such as target deformation, target fracture, or as a transfer of momentum. The particular function being performed will dictate which of these results is most adaptive to the organism. Chewing food favors fracture, whereas running favors the transfer of momentum from the appendages to the ground. Here, we explore the relationship between deformation, fracture, and momentum transfer in biological puncture systems. Puncture is a widespread behavior in biology requiring energy transfer into a target to allow fracture and subsequent insertion of the tool. Existing correlations between both tool shape and tool dynamics with puncture success do not account for what energy may be lost due to deformation and momentum transfer in biological systems. Using a combination of pendulum tests and particle tracking velocimetry (PTV), we explored the contributions of fracture, deformation and momentum to puncture events using a gaboon viper fang. Results on unrestrained targets illustrate that momentum transfer between tool and target, controlled by the relative masses of the two, can influence the extent of fracture achieved during high-speed puncture. PTV allowed us to quantify deformation throughout the target during puncture and tease apart how input energy is partitioned between deformation and fracture. The relationship between input energy, target deformation and target fracture is non-linear; increasing impact speed from 2.0 to 2.5 m/s created no further fracture, but did increase deformation while increasing speed to 3.0 m/s allowed an equivalent amount of fracture to be achieved for less overall deformation. These results point to a new framework for examining puncture systems, where the relative resistances to deformation, fracture and target movement dictate where energy flows during impact. Further developing these methods will allow researchers to quantify the energetics of puncture systems in a way that is comparable across a broad range of organisms and connect energy flow within an organism to how that energy is eventually transferred to the environment.

It makes intuitive sense that you need a sharp tool to puncture through a tough material. The typical approach to evaluating sharpness in biological puncturing tools is to treat morphological measurements as a proxy for puncture ability. However, there are multiple approaches to measuring sharpness, and the relative influence of morphology on function remains unclear. Our goal is to determine what aspects of tip morphology have the greatest impact on puncture ability, using (a) viper fangs and (b) engineered punches to isolate the effects of different sharpness measures. Our results indicate that tip included angle is the strongest predictor of puncture performance in both viper fangs and engineered punches. For puncture tools with small included angles, sharpness index (based on the radius of curvature) also affects puncture ability. Finally, we found that punches serve as good predictors of fang performance at small angles and sharpness index values.

The similarities between ichthyosaurs and sharks are a text-book example of convergence, and similarities in tail morphology have led many to theorize that they had similar swimming styles. The variation of ichthyosaur tail shapes is encompassed within the diversity of shark families. In particular early ichthyosaurs have asymmetrical tails like the heterocercal tails of carcharhinid sharks, while later occurring ichthyosaurs have lunate tails similar to those of lamnid sharks. Because it is not possible to measure ichthyosaur tail function, the goal of this study is to measure and compare the flexibility and stiffness of lunate and heterocercal shark tails, and to measure skeletal and connective tissue features that may affect tail flexibility. We measured flexibility in 10 species and focused on five species in particular, for dissection: one pelagic and one bottom-associated individual from each order, plus the common thresher shark (Die Ähnlichkeiten zwischen Ichthyosauriern und Haien ist ein Lehrbuchbeispiel für Konvergenz, und Ähnlichkeiten in der Schwanzflossenmorphologie haben zu der Theorie geführt, dass beide ähnliche Schwimmstile aufwiesen. Die Formvielfalt der Ichthyosaurier-Schwanzflossen findet ihre Entsprechung innerhalb der Diversität der Schwanzflossen von Haifamilien. Frühe Ichthyosaurier beispielsweise, zeigen asymmetrische Schwanzflossen ähnlich den heterocerken Schwanzflossen von Requiemhaien (Carcharhinidae), während später auftretende Ichthyosaurier lunulare Schwanzflossen aufweisen, ähnlich denen von Makrelenhaiartigen (Lamniformes). Da es unmöglich ist, die Schwanzflosse der Ichthyosaurier auf ihre Funktion hin zu untersuchen, besteht das Ziel dieser Studie darin, die Flexibilität und Steifheit von lunularen und heterocerken Hai-Schwanzflossen zu messen und zu vergleichen, sowie Merkmale von Skelett- und Bindegewebe zu bestimmen, die möglicherweise die Flexibilität der Schwanzflosse beeinflussen. Wir haben die Flexibilität bei 10 Arten bestimmt, wobei wir uns beim Sezieren auf fünf Arten konzentriert haben: ein pelagisches und ein bodenassoziiertes Individuum aus jeder Ordnung sowie den gemeinen Fuchshai (Alopias vulpinus), ein Spezialist für ‚tail-flapping‘(Einsetzen der Schanzflosse gegen Beutefische). Wie erwartet waren lunulare Schwanzflossen insgesamt weniger flexibel als heterocerke und wiesen eine höhere Biegesteifigkeit auf. Unsere Ergebnisse deuten darauf hin, dass das Querschnittsprofil des skelettgestützten des dorsalen Lobus die Biegesteifigkeit bedingt, wohingegen die Veränderung der Gewebezusammensetzung maßgeblich ist für die Biegesteifigkeit des ventralen Lobus. Zudem fanden wir strukturelle Unterschiede, die das Schwanzschlagverhalten (‚tail-flapping‘) des gemeinen Fuchshais ermöglichen könnten. Abschließend diskutieren wir unsere morphologischen Messungen im Vergleich mit Ichthyosaurier-Messungen aus der Literatur. Unter besonderer Berücksichtigung der Ähnlichkeiten in der funktionellen Morphologie als Stütze für die These, dass Haie ein gutes Analogon zum Verständnis der Ichthyosaurus-Schwimmbiomechanik sind. (By S. Kruppert)As semelhanças entre ictiossauros e tubarões são um exemplo clássico de convergência e semelhanças na morfologia da cauda levaram muitos a teorizar que eles tinham estilos de natação semelhantes. A variação das formas da cauda do ictiossauro é encontrada nas diversas famílias de tubarões. Em particular, os primeiros ictiossauros têm caudas assimétricas, como as caudas heterocercas dos tubarões carcharhinídeos, enquanto os ictiossauros, mais tarde, adquirem caudas semilunares semelhantes às dos tubarões lamnídeos. Como não é possível medir a função da cauda do ictiossauro diretamente, o objetivo deste estudo é medir e comparar a flexibilidade e a rigidez das caudas lunadas e heterocercas de tubarões e medir as características do tecido esquelético e conectivo que podem afetar a flexibilidade delas. Nós medimos a flexibilidade em 10 espécies e focamos em cinco delas para dissecação: um indivíduo pelágico e um indivíduo bentônico de cada ordem, além do tubarão-raposa (Alopias vulpinus), um especialista em chicoteio de cauda. Como esperado, as caudas semilunares eram geralmente menos flexíveis que as caudas heterocercas e tinham maior resistência à flexão. Nossos resultados sugerem que o perfil transversal do lobo dorsal com suporte esquelético determina a capacidade de flexão, mas que a alteração da composição do tecido determina a capacidade de flexão no lobo ventral. Também encontramos diferenças estruturais que podem possibilitar o comportamento de chicoteio na cauda do tubarão-raposa. Finalmente, discutimos como nossas medições morfológicas se comparam às dos ictiossauros encontradas na literatura, notando que similaridades na morfologia funcional sugerem que os tubarões podem ser um bom análogo para a compreensão da biomecânica da natação do ictiossauro. (By G. Sobral).इक्थियोसॉरस और शार्क के बीच समानताएं अभिसरण का एक पाठ्य-पुस्तक उदाऴरण ऴैं, और ईनकी पूंछ आकृति विज्ञान की समानता ने कई लोगों को यऴ सिद्ध करने के लिए प्रेरित किया ऴै कि ईनके पास समान तैराकी शैली थी। शार्क के परिवारों की विविधता के भीतर इचिथियोरस पूंछ की आकृतियों की विविधता को शामिल किया गया ऴै। विशेष रूप से शुरुआती इक्थियोसॉरस के पास विषम आकार की पूंछें ऴोती थी जैसे कि कार्सरिनिड शार्क की विषमकोणीय आकार की पूंछ, जबकि बाद में ऴोने वाले इक्थियोसॉरस के पास लैम्निड शार्क के समान लसीली (लूनेट) पूंछ ऴोती थी। क्योंकि इचिथियॉर्स की पूंछ के कृत्य को मापना संभव नऴीं ऴै, इस अध्ययन का लक्ष्य ऴै कि लूनेट और ऴेटेरोसेरेल शार्क की पूंछ के लचीलेपन और कठोरता की माप करना और तुलना करना, और कंकालीय संयोजी ऊतक विशेषताओं को मापना जो पूंछ के लचीलेपन को प्रभावित कर सकते ऴैं। ऴमने 10 प्रजातियों के लचीलेपन को मापा, और विशेष रूप से विच्छेदन के लिए पांच प्रजातियों पर ध्यान केंद्रित किया: एक पेलजिक प्रजाति, एक नीचे से जुड़ा ऴुआ प्रजाति, और साथ ऴी एक पूंछ-थप्पड़ विशेषज्ञ जैसे कि सामान्य थ्रेशर शार्क (एलोपियास वल्पिनस)। जैसी कि उम्मीद थी, कुल मिलाकर लूनेट शार्क की पूंछ ऴेटेरोसेरेल पूंछ की तुलना में कम लचीली थी और इसमें अधिक लचीली कठोरता थी। ऴमारे परिणामों से पता चलता ऴै कि कंकाल के समर्थित पृष्ठीय लोब का पार-अनुभागीय प्रोफ़ाइल फ्लेक्सुरल कठोरता को निर्धारित करता ऴै, लेकिन यऴ कि ऊतक संरचना को बदलने से वेंट्रल लोब में फ्लेक्सुरल कठोरता का निर्धारण ऴोता ऴै। ऴमने संरचनात्मक अंतर भी पाया जो सामान्य थ्रेशर शार्क के पूंछ के थप्पड़ व्यवऴार को सक्षम कर सकता ऴै। अंत में, ऴम चर्चा करते ऴैं कि ऴमारे आकृति विज्ञान के माप साऴित्य से इक्थियोसॉरस माप की तुलना कैसे करते ऴैं। अथार्थ कार्यात्मक आकृति विज्ञान में मौजूदा समानताएं बताती ऴैं कि शार्क इक्थियोसॉरस तैराकी की जैव यांत्रिकी को समझने के लिए एक अच्छा सादृश्य ऴो सकता ऴै। (By S. K. Ray).

Spines are common morphological features found in almost all major biological groups offering an opportunity to explore large-scale evolutionary convergence across disparate clades. As an example, opuntioid cacti have spines with barbed ornamentation that is remarkably similar in form and scale to that found on porcupine quills, suggesting specific biomechanical convergence across the animal and plant kingdoms. While the mechanics of porcupine quills as defensive mechanisms has been previously tested, the mechanics of cactus spines (which have evolved to fill a number of functions including defence, climbing and dispersal) has not been characterized. Here we study the puncturing and anchoring ability of six species of cactus, including both barbed and non-barbed spines. We found that barbed spines require less work to puncture a variety of targets than non-barbed spines. Barbed spines also require more work than non-barbed spines to withdraw from biological materials, owing to their barbs engaging with tissue fibres. These results closely match those found previously for barbed versus non-barbed porcupine quills, implying biomechanical convergence. The variation in performance of barbed versus non-barbed spines, as well as between barbed spines from different species, is probably tied to the diversity of ecological functions of cactus spines.

Polyplacophoran molluscs show low morphological diversity compared to other marine invertebrate clades, yet chitons are ecologically important grazers that occupy a range of distinct ecological niches. We investigated a potential functional correlate of niche separation in three species of co-occurring mopallid chitons that have total ranges across differing environments (Mopalia muscosa, Mopalia lignosa, Katharina tunicata). We found that the force needed to fracture the protective valves varied significantly among species. K. tunicata, whose valves have a relatively reduced exposed dorsal surface, was significantly more resistant to fracture than the two Mopalia species (mean force: K. tunicata = 31.9 ± 4.5 N; M. lignosa = 12.5 ± 0.8 N; M. muscosa = 20.2 ± 0.8 N). In Mopalia spp., the terminal valves were significantly stronger than intermediate valves (i.e. higher force to fracture), whereas all valves in K. tunicata appeared to be functionally equivalent. To assess whether future chemical changes predicted under ocean acidification (OA) will affect these species differently, we measured the force to fracture of valves after 10 days of exposure to elevated pCO2 (control = 8.0 pH [407 ± 104, pCO2], elevated = 7.5 pH [1544 ± 249, pCO2]) for both live animals and dissected individual valves. Although previous experimental OA work found significant impacts of elevated pCO2 on adult mollusc shells over similar timescales, we saw no reduction in total strength related to treatment. Our data demonstrate that diversity in chiton valve morphology has functional implications and that physical changes in local topology and wave exposure may have stronger impacts on adult chitons than changes in ocean chemistry under future climate change.

In addition to breaking hard prey items, the teeth of durophagous predators must also resist failure under high loads. To understand the effects of morphology on tooth resistance to failure, finite element models were used to examine differences in total strain energy (J), first principal strain, and the distribution of strains in a diversity of canonical durophagous tooth morphologies. By changing the way loads were applied to the models, I was also able to model the effects of large and small prey items. Tooth models with overall convex morphologies have higher in-model strains than those with flat or concave occlusal surface. When a cusp is added to the tooth model, taller or thinner cusps increase in-model strain. While there is little difference in the relationships between tooth morphology and strain measurements for most models, there is a marked difference between effects of the large and small prey loads on the concave and flat tooth morphologies. Comparing these data with measurements of force required by these same morphologies to break prey items illustrates functional tradeoffs between the need to prevent tooth failure under high loads by minimizing in-tooth strain versus the drive to reduce the total applied force.

All stingrays in the family Myliobatidae are durophagous, consuming bivalves and gastropods, as well as decapod crustaceans. Durophagous rays have rigid jaws, flat teeth that interlock to form pavement-like tooth plates, and large muscles which generate bite forces capable of fracturing stiff biological composites (e.g., mollusk shell). The relative proportion of different prey types in the diet of durophagous rays varies between genera with some stingray species specializing on particular mollusk taxa, while others are generalists. The tooth plate module provides a curved occlusal surface on which prey is crushed, and this curvature differs significantly among myliobatids. We measured the effect of jaw curvature on prey-crushing success in durophagous stingrays. We milled aluminum replica jaws rendered from computed tomography scans, and crushed live mollusks, 3D printed gastropod shells, and ceramic tubes with these fabricated jaws. Our analysis of prey items indicate that gastropods were consistently more difficult to crush than bivalves (i.e. were stiffer), but that mussels require the greatest work-to-fracture. We found that replica shells can provide an important proxy for investigations of failure mechanics. We also found little difference in crushing performance between jaw shapes, suggesting that disparate jaws are equally suited for processing different types of shelled prey. Thus, durophagous stingrays exhibit a many-to-one mapping of jaw morphology to mollusk crushing performance.

Organisms that are durophagous, hard prey consumers, have a diversity of tooth forms. To determine why we see this variation, we tested whether some tooth forms break shells better than others. We measured the force needed with three series of aluminium tooth models, which varied in concavity and the morphology of a stress concentrating cusp, to break a shell. We created functionally identical copies of two intertidal snail shells: the thicker shelledNucella ostrinaand the more ornamentedNucella lamellosausing a three-dimensional printer. In this way, we reduced variation in material properties between test shells, allowing us to test only the interaction of the experimental teeth with the two shell morphologies. We found that for all tooth shapes, thicker shells are harder to break than the thinner shells and that increased ornamentation has no discernible effect. Our results show that for both shell morphologies, domed and flat teeth break shells better than cupped teeth, and teeth with tall or skinny cusps break shells best. While our results indicate that there is an ideal tooth form for shell breaking, we do not see this shape in nature. This suggests a probable trade-off between tooth function and the structural integrity of the tooth.

Here, we document in-vivo bite forces recorded from wild piranhas. Integrating this empirical data with allometry, bite simulations, and FEA, we have reconstructed the bite capabilities and potential feeding ecology of the extinct giant Miocene piranha, Megapiranha paranensis. An anterior bite force of 320 N from the black piranha, Serrasalmus rhombeus, is the strongest bite force recorded for any bony fish to date. Results indicate M. paranensis' bite force conservatively ranged from 1240-4749 N and reveal its novel dentition was capable of resisting high bite stresses and crushing vertebrate bone. Comparisons of body size-scaled bite forces to other apex predators reveal S. rhombeus and M. paranensis have among the most powerful bites estimated in carnivorous vertebrates. Our results functionally demonstrate the extraordinary bite of serrasalmid piranhas and provide a mechanistic rationale for their predatory dominance among past and present Amazonian ichthyofaunas.

The sandfish, a type of desert lizard, can vanish into a sandy substrate in a blink of an eye. Approaches that draw on mathematics, physics and engineering provide complementary insights into how the animal achieves this feat.

The Q-cycle mechanism of the bc1 complex explains how the electron transfer from ubihydroquinone (quinol, QH2) to cytochrome (cyt) c (or c2 in bacteria) is coupled to the pumping of protons across the membrane. The efficiency of proton pumping depends on the effectiveness of the bifurcated reaction at the Q(o)-site of the complex. This directs the two electrons from QH2 down two different pathways, one to the high potential chain for delivery to an electron acceptor, and the other across the membrane through a chain containing heme bL and bH to the Qi-site, to provide the vectorial charge transfer contributing to the proton gradient. In this review, we discuss problems associated with the turnover of the bc1 complex that center around rates calculated for the normal forward and reverse reactions, and for bypass (or short-circuit) reactions. Based on rate constants given by distances between redox centers in known structures, these appeared to preclude conventional electron transfer mechanisms involving an intermediate semiquinone (SQ) in the Q(o)-site reaction. However, previous research has strongly suggested that SQ is the reductant for O2 in generation of superoxide at the Q(o)-site, introducing an apparent paradox. A simple gating mechanism, in which an intermediate SQ mobile in the volume of the Q(o)-site is a necessary component, can readily account for the observed data through a coulombic interaction that prevents SQ anion from close approach to heme bL when the latter is reduced. This allows rapid and reversible QH2 oxidation, but prevents rapid bypass reactions. The mechanism is quite natural, and is well supported by experiments in which the role of a key residue, Glu-295, which facilitates proton transfer from the site through a rotational displacement, has been tested by mutation.