Romain David

Implementing and Innovating Marine Monitoring Approaches for Assessing Marine Environmental Status

Marine environmental monitoring has tended to focus on site-specific methods of investigation. These traditional methods have low spatial and temporal resolution and are relatively labor intensive per unit area/time that they cover. To implement the Marine Strategy Framework Directive (MSFD), European Member States are required to improve marine monitoring and design monitoring networks. This can be achieved by developing and testing innovative and cost-effective monitoring systems, as well as indicators of environmental status. Here, we present several recently developed methodologies and technologies to improve marine biodiversity indicators and monitoring methods. The innovative tools are discussed concerning the technologies presently utilized as well as the advantages and disadvantages of their use in routine monitoring. In particular, the present analysis focuses on: (i) molecular approaches, including microarray, Real Time quantitative PCR (qPCR), and metagenetic (metabarcoding) tools; (ii) optical (remote) sensing and acoustic methods; and (iii) in situ monitoring instruments. We also discuss their applications in marine monitoring within the MSFD through the analysis of case studies in order to evaluate their potential utilization in future routine marine monitoring. We show that these recently-developed technologies can present clear advantages in accuracy, efficiency and cost.

Assessing morphology and function of the semicircular duct system: introducing new in-situ visualization and software toolbox

The semicircular duct system is part of the sensory organ of balance and essential for navigation and spatial awareness in vertebrates. Its function in detecting head rotations has been modelled with increasing sophistication, but the biomechanics of actual semicircular duct systems has rarely been analyzed, foremost because the fragile membranous structures in the inner ear are hard to visualize undistorted and in full. Here we present a new, easy-to-apply and non-invasive method for three-dimensional in-situ visualization and quantification of the semicircular duct system, using X-ray micro tomography and tissue staining with phosphotungstic acid. Moreover, we introduce Ariadne, a software toolbox which provides comprehensive and improved morphological and functional analysis of any visualized duct system. We demonstrate the potential of these methods by presenting results for the duct system of humans, the squirrel monkey and the rhesus macaque, making comparisons with past results from neurophysiological, oculometric and biomechanical studies. Ariadne is freely available at http://www.earbank.org.

Morphology and function of Neandertal and modern human ear ossicles

Significance Middle ear ossicles are critical for audition and rarely preserved in fossils. Based on microcomputed tomography images, our comparative 3D shape analysis of Neandertal ossicles shows striking shape differences between Neandertals and anatomically modern humans (AMHs). However, these morphological differences do not affect the functional properties of the ossicles, potentially indicating consistent aspects of vocal communication in Neandertals and AMHs. Instead, a strong relationship between ossicle morphology and tympanic cavity architecture is found. The diminutive middle ear ossicles (malleus, incus, stapes) housed in the tympanic cavity of the temporal bone play an important role in audition. The few known ossicles of Neandertals are distinctly different from those of anatomically modern humans (AMHs), despite the close relationship between both human species. Although not mutually exclusive, these differences may affect hearing capacity or could reflect covariation with the surrounding temporal bone. Until now, detailed comparisons were hampered by the small sample of Neandertal ossicles and the unavailability of methods combining analyses of ossicles with surrounding structures. Here, we present an analysis of the largest sample of Neandertal ossicles to date, including many previously unknown specimens, covering a wide geographic and temporal range. Microcomputed tomography scans and 3D geometric morphometrics were used to quantify shape and functional properties of the ossicles and the tympanic cavity and make comparisons with recent and extinct AMHs as well as African apes. We find striking morphological differences between ossicles of AMHs and Neandertals. Ossicles of both Neandertals and AMHs appear derived compared with the inferred ancestral morphology, albeit in different ways. Brain size increase evolved separately in AMHs and Neandertals, leading to differences in the tympanic cavity and, consequently, the shape and spatial configuration of the ossicles. Despite these different evolutionary trajectories, functional properties of the middle ear of AMHs and Neandertals are largely similar. The relevance of these functionally equivalent solutions is likely to conserve a similar auditory sensitivity level inherited from their last common ancestor.

Comparative anatomy of the middle ear ossicles of extant hominids – Introducing a geometric morphometric protocol

The presence of three interconnected auditory ossicles in the middle ear is a defining characteristic of mammals, and aspects of ossicle morphology are related to hearing sensitivity. However, analysis and comparison of ossicles are complicated by their minute size and complex three-dimensional shapes. Here we introduce a geometric morphometric measurement protocol for 3D shape analysis based on landmarks and semilandmarks obtained from μCT images and apply it to ossicles of extant hominids (great apes and humans). We show that the protocol is reliable and reproducible over a range of voxel resolutions, and captures even subtle shape differences. Using this approach it is possible to distinguish the hominid taxa by mean shapes of their malleus and incus (p < 0.01). The stapes appears less diagnostic, although this may in part be related to the small sample size available. Using ancestral state estimation, we show that, within hominids, Homo sapiens is derived with respect to its malleus (short manubrium, long corpus, head anterior-posterior flattened, articular facet shape), incus (wide intercrural curvature, long incudal processes, articular facet shape) and stapes (high stapes with kidney-shaped footplate). H. sapiens also shows a number of plesiomorphic shape traits whereas Gorilla and Pan possess a number of autapomorphic characteristics. The Pongo ossicles appear to be close to the plesiomorphic hominid condition. The malleus shows little difference in size among hominids, and allometry is thus of little importance. In contrast, the incus and stapes are more variable in size, and their shape is more strongly related to size differences. Although the form-function relationships in the middle ear are not fully understood, some aspects of ossicle morphology suggest that interspecific differences in hearing capacities are present among hominids. Finally, the results of this study provide a comparative framework for morphometric studies analyzing ossicles of extinct hominids, with a bearing on taxonomy, phylogeny and auditory function.

A multispecies approach reveals hot spots and cold spots of diversity and connectivity in invertebrate species with contrasting dispersal modes

Genetic diversity is crucial for species’ maintenance and persistence, yet is often overlooked in conservation studies. Species diversity is more often reported due to practical constraints, but it is unknown if these measures of diversity are correlated. In marine invertebrates, adults are often sessile or sedentary and populations exchange genes via dispersal of gametes and larvae. Species with a larval period are expected to have more connected populations than those without larval dispersal. We assessed the relationship between measures of species and genetic diversity, and between dispersal ability and connectivity. We compiled data on genetic patterns and life history traits in nine species across five phyla. Sampling sites spanned 600 km in the northwest Mediterranean Sea and focused on a 50‐km area near Marseilles, France. Comparative population genetic approaches yielded three main results. (i) Species without larvae showed higher levels of genetic structure than species with free‐living larvae, but the role of larval type (lecithotrophic or planktotrophic) was negligible. (ii) A narrow area around Marseilles, subject to offshore advection, limited genetic connectivity in most species. (iii) We identified sites with significant positive contributions to overall genetic diversity across all species, corresponding with areas near low human population densities. In contrast, high levels of human activity corresponded with a negative contribution to overall genetic diversity. Genetic diversity within species was positively and significantly linearly related to local species diversity. Our study suggests that local contribution to overall genetic diversity should be taken into account for future conservation strategies.

Secret laws of the labyrinth

This abstract presents new results on the structure and function of vestibular part of the inner ear of vertebrates with special emphasis on human behavior. First we summarize a mathematical analysis of motion of the endolymphatic fluid, justifying known approximated formulas for the cupula functioning based on a set of anatomical parameters. Some of these parameters can be estimated from the bony labyrinth, some others cannot be. We present original data issued from synchrotron microtomography (Sμ CT) of five tetrapod species, allowing to compare bony and membranous labyrinths. We derive several simple and robust empirical laws connecting membranous parameters and bony parameters. Then, using published results on human labyrinths (Bradshaw et al. 2009), we deduce functional consequences for the human labyrinths. For instance we show that, contrarily to current belief, the kinematic sensitivity for yaw is larger than for pitch and roll.

Shape and function of the hominid auditory region

Intergroup encounters can have a substantial impact on individual fitness by altering access to resources and increasing risk of injury and death. Numerical advantage is usually of para- mount importance to maintain access to resources in between group contests. However, factors affecting payoffs can also be involved in determining intergroup encounter outcome and inten- sity. The most investigated so far has been location, often found to be relevant in explaining contest result and level of aggression. Other factors, such as proportion of infants and female reproductive state have yet to be thoroughly examined. Our aim was to investigate whether fe- male reproductive state and proportion of infants, together with group size and location, played a role in determining the outcome and intensity of intergroup encounters. We collected data for 9 consecutive months on 3 habituated groups of crested macaques ( Macaca nigra ) in the Tang- koko Nature Reserve (North Sulawesi, Indonesia), yielding information on 163 intergroup en- counters. Encounters tended to finish in a draw when groups were of similar sizes and both used the location of the encounter with similar frequency. Odds of winning an encounter (i.e. displac- ing the other group) were higher for those groups that used the encounter area more frequently and had lower proportions of both fertile females and females with infants. The longer the en- counter, the more likely it was to be aggressive, especially when group sizes were similar. Our data support previous findings that location and group size play an important role in determin- ing the nature and outcome of encounters. However, they suggest that intergroup encounters are influenced by a broad range of factors that affect the competitive ability of groups. Our study provides evidence that intergroup relationships in primates are more context dependent than previously thought.Lemur Abundance in the Lowland Rainforest of Tsitongambarika, Southeastern Madagascar : Altitudinal and Latitudinal ComparisonsBiomechanical analyses of great ape arboreal locomotion in a natural environment are scarce, thus limiting attempts to correlate behavioural and habitat differences with variation in skeletal morphology. Vertical climbing is a crucial locomotor and foraging strategy of great apes and the hands are critically important to maintaining stability on irregular, arboreal substrates. However, little is known about arboreal grips and hand postures, or how these might vary with forelimb posture during vertical climbing on natural substrates of different sizes. This is particularly true of mountain gorillas, which are considered the least arboreal of all African apes and for which the characteristics of vertical climbing have not yet been studied. The aim of this study was to compare temporal kinematics of hand and forelimb use during vertical climbing in wild, habituated mountain gorillas (Gorilla beringei beringei) of the Bwindi Impenetrable Forest (Uganda) and sanctuary chimpanzees (Pan troglodytes) of the Chimfunshi Wildlife Orphanage Trust (Zambia) to assess differences in climbing styles that may relate to variation in hand or forelimb morphology and body mass. We investigated hand and forelimb posture coupled with temporal gait parameters during vertical climbing (both ascent and descent) in 15 mountain gorillas and eight chimpanzees, using video records ad libitum. In both apes, forelimb posture was correlated with substrate size during both ascent and descent climbing. Both apes used power grips and a diagonal power grip, involving three different thumb postures. Gorillas showed greater ulnar deviation of the wrist during climbing than chimpanzees, and the thumb played an important supportive role when vertically descending compliant substrates in gorillas. Comparisons of temporal gait parameters indicated that large-bodied gorillas exhibited significant longer cycle duration, lower stride frequency and generally a higher duty factor than chimpanzees. This study revealed that wild mountain gorillas adapt their climbing strategy to accommodate their large body mass in a similar manner found in captive western lowland gorillas, but that our sanctuary chimpanzees showed less variation in their climbing strategy within a natural environment than has been documented in captive bonobosMany primates face spatial and temporal fluctuations in food availability, which can significantly affect their ability to meet nutritional requirements. Anthropogenic disturbances and influences, such as agriculture, human presence and infrastructures, can further impact seasonal food availability, dietary composition and nutrition. Primates residing in anthropogenic landscapes often incorporate cultivars into their diets. However, the nutritional drivers behind cultivar consumption are poorly understood. We examined variations in chimpanzee (Pan troglodytes verus) macronutrient intake from wild and cultivated foods between sexes and seasons over a 1year period in Bossou, Guinea. We used the geometric framework of nutrition to examine proportional contributions of macronutrients to the diet and nutrient balancing. We conducted continuous focal observations of adult individuals ( n = 10) to record all feeding bouts and conducted nutritional analyses of plant foods (25 wild species; 11 cultivated species). We found no sex differences in chimpanzees for wild or cultivated food or macronutrient intakes; however, females showed higher intakes of total food (i.e. wild and cultivated combined), digestible fibre (NDF), and protein when controlling for metabolic body mass. There were no differences in wild or cultivated food intake between seasons; however, lipid and protein intake from cultivars were higher when wild fruit availability was low. Chimpanzees maintained a constant proportional intake of protein while allowing carbohydrates and lipid intakes to vary. Furthermore, they were able to maintain a consistent balance of protein to non-protein (carbohydrates, lipids, and NDF) energy across the year. Our results suggest that Bossou chimpanzees suffered little seasonal constraints in food quality or availability since they were able to combine their consumption of available wild and cultivated foods to achieve a balanced diet. These findings contribute significantly to our understanding of primate nutritional requirements and their ability to meet these in disturbed environments.

CIGESMED : Coralligenous based Indicators to evaluate and monitor the "Good Environmental Status" of the Mediterranean coastal waters

Melih Ertan CINAR1, FERAL2 J-P., ARVANITIDIS3 C., DAVID2 R., TAŞKIN4 E., DAILIANIS3 T., DOĞAN1 A., GEROVASILEIOU5 V., DAĞLI1 E., AYSEL6 V., ISSARIS3 Y., BAKIR1 K., SALOMIDI3 M., SINI5 M., ACIK6 S., EVCEN1 A., DIMITRIADIS5 C., KOUTSOUBAS5 D., SARTORETTO7 S., ONEN1 S. and with contributors* 1 Ege University, Faculty of Fisheries, Izmir, Turkey; 2CNRS-IMBE, France; 3HCMR, Greece; 4CBU, Turkey; 5NMPZ, Greece; 6DEU, Turkey; 7IFREMER, France *(list on www.cigesmed.eu)