Comparative analysis of the jaw apparatus of three marine annelids using scanning electron microscopy: Microstructure and elemental composition

Abstract

Polychaeta are highly diversified invertebrates that inhabit marine, brackish or freshwater environments. They have acquired a unique range of adaptative features for securing food. However, the jaw apparatus may reveal not only defence and predation mechanisms, but also its relation to environmental chemistry. The present work compared the structure and chemical profile of the jaws of different estuarine Polychaeta: Nephtys hombergii (Nephtyidae), Hediste diversicolor (Nereididae) and Glycera alba (Glyceridae) using Scanning Electron Microscopy (SEM) and Scanning Electron Microscopy with Energy Dispersive X‐Ray (SEM–EDX). Analyses revealed that N. hombergii possesses a muscular jawless proboscis with terminal sensorial papillae for detecting prey, whereas the G. alba proboscis exhibits four delicately sharp jaws with perforations for venom delivery and H. diversicolor bears two blunt denticulated jaws to grasp a wide variety of food items. Melanin and metals like copper provide hardness to the slender jaws of Glycera, while, in the absence of heavier metallic elements, halogens contribute to H. diversicolor jaws robustness. The more specific chemistry of the jaws of glycerids is associated with its more refined venom injection, whereas Hediste is an opportunistic omnivore and Nepthys an agile forager. Altogether, the chemistry of jaws is an adaptive feature for feeding, locomotion and even resilience to complex and often adverse chemical profiles of estuaries.

The chemistry of jaws is an adaptive feature for feeding, locomotion and even resilience to complex and often adverse chemical profiles of estuaries. The jaw structure and shape are strongly linked with the different feeding modes, as well the ecology of each species of Polychaeta. The elemental composition revealed that mandible hardness may be dependent on the presence of specific elements in these structures.

1. INTRODUCTION

The Polychaeta belong to one of most represented and diversified phyla among marine animals, the Annelida. With more than 11,400 validated species of polychaetes in the present day, this group of aquatic invertebrates occupies both freshwater and marine environments, and in the latter case, from intertidal pools to deep‐sea vents, being key elements in the ecological structure of these habitats, particularly benthic environments (Hayward & Ryland, 2017; Pamungkas et al., 2019). These abundant organisms are important elements of trophic webs as primary consumers, predators and detritivores, not to mention commensals and parasites, and are even associated with primary producers like the beardworm Riftia pachyptila of deep‐sea hydrothermal vents, a species that hosts chemoautotrophic bacteria. This is reflected in highly diverse modes of feeding, including deposit feeders, filter feeders, carnivores and omnivores (Fauchald & Jumars, 1979). Such diverse modes of feeding imply several morphological adaptations that can mean, for instance, the presence or absence of jaws as well as different types of sense organs (e.g., palps, antennae, tentacular cirri, nuchal organs, eyes, pharyngeal papillae) that can be more or less specialised depending on species and many of which are not yet fully understood.

Trophic relationships aside, the Polychaeta play other highly relevant roles in their environment. Besides being prey for fish, larger invertebrates and birds, the close association between these animals and the benthic milieu renders them especially relevant in monitoring for marine pollution. It must be noted that many inhabit highly impacted habitats such as estuaries, appearing to be highly resilient in areas contaminated by metals, organic or organometallic compounds. Thus, Polychaeta can be studied to assess the direct impact of anthropogenic activities, like aquaculture, for instance, which can have a high impact in benthic communities (see Dean, 2008 and Sanchis et al., 2021, plus Rodrigo & Costa, 2019, for a review). Since their habitats range from the water column to sediments, polychaetes have been long employed in ecotoxicological and biomonitoring studies in part because their resilience in contaminated environments may reflect specific physiological mechanisms to cope with chemical challenge. One important example is the case of the ability of some species to detoxify halogenated compounds, metals or metalloids (Dean, 2008; Fielman et al., 1999; Mouneyrac et al., 2003). Although it is proposed that detoxification could be associated with biomineralisation processes in invertebrates, there is no clear evidence whether its regulation in polychaetes is dependent on environmental chemical profiles or it is highly species‐specific (Mouneyrac et al., 2003; Simkiss, 1977). In general, this process is very little studied. Understanding these processes can have important implications for biomonitoring and bioremediation in impacted sites.

As a contribution to study biomineralisation in Polychaeta and its relation to feeding ecology, the present work aimed at investigating the relationship between the microanatomy and the elemental profiles of the jaw apparatus of different estuarine polychaetes representative of the Western European Atlantic estuarine environment, namely: Nephtys hombergii (Nephtyidae), Hediste diversicolor (Nereididae) and Glycera alba (Glyceridae). These are regarded as sympatric species with distinct foraging and feeding behaviours, being considered sensitive to environmental stressors such pollution and overall water quality. They can, therefore, be exposed to the same chemical environment.

2. MATERIALS AND METHODS

2.1. Animal collection

Between March and May 2019, three species of marine polychaetes, Nephtys hombergii (Nephtyidae), Hediste diversicolor (Nereididae) and Glycera alba (Glyceridae) were hand‐collected from estuarine areas of the Portuguese West coast. The collection sites consisted of sandy beaches (Tróia peninsula, 38°28′14.4″ N, 8°52′05.0″ W) and estuarine mudflats (Alcochete, 38°45′40.1″ N, 8°56′08.1″ W and Seixal, 38°38′41.7″ N, 9°06′08.2″ W). N. hombergii, H. diversicolor and G. alba were collected from Tróia peninsula, Alcochete and Seixal, respectively (Figure 1). Animals were transported alive to the laboratory for taxonomic identification and tissue harvesting.

FIGURE 1.

Estuarine sampling areas for annelids. Tróia (Nephtys hombergii), sandy; Seixal (Glycera alba) and Alcochete (Hediste diversicolor), mudflats.

2.2. Sample preparation

Samples were immediately fixed with 2.5% v/v glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.4). Fixation was performed at room temperature for 2 h. Samples were then washed in cacodylate buffer (3 × 15 min), followed by dehydration according to the method described by Inoué and Osatake (1988) and adapted by Rodrigo et al. (2018). In brief, samples were dehydrated through progressive series of (aqueous) ethanol (30–100% v/v), infiltrated with tert‐butanol (3 × 15 min, at 40°C) and allowed to freeze overnight at 4°C. Before both Scanning Electron Microscopy (SEM) and Scanning Electron Microscopy with Energy Dispersive X‐Ray (SEM–EDX) analyses, tert‐butanol was sublimated under vacuum until complete dryness.

2.3. Scanning electron microscopy analyses (SEM and SEM–EDX)

Prior to the analysis, the samples were mounted on an aluminium disc using a double‐sided adhesive carbon tape and coated with chromium (N. hombergii and H. diversicolor) and carbon (G. alba) using a JEOL JEE‐400 vacuum evaporator. Mandible elements identification was only performed for species with visible mandibles after its proboscis eversion, namely, G. alba and H. diversicolor. Elemental mapping was performed using a Bruker Nano GmbH XFlash detector 610 M. Both SEM and SEM–EDX analyses were performed in a JEOL JSM‐5400 Scanning Microscope, operated between 10 and 20 keV, using the ESPRIT Compact Software version 2.1.

3. RESULTS

The main characteristics of the buccal apparatus of Nephtys hombergii, Glycera alba and Hediste diversicolor are summarised in Table 1. In this respect, Nephtys hombergii differs from Hediste diversicolor and Glycera alba by not having extrudable jaws. From its small and pentagonal‐shaped prostomium, N. hombergii everts its comparatively larger and densely muscular proboscis (pharynx) that is fitted with several longitudinal rows of subterminal papillae and a middorsal papilla (Figure 2a,b). The proboscis is tipped by 10 pairs of soft and bifid (bifurcate) terminal papillae surrounding the buccal cavity (Figure 2c,d).

TABLE 1.

Summary of the main characteristics of buccal apparatus of Nephtys hombergii, Glycera alba and Hediste diversicolor.

	Nephtys hombergii	Glycera alba	Hediste diversicolor	References
Feeding behaviour	Motile predator, carnivorous	Ambush predator, carnivorous	Opportunistic predator, omnivorous	Arndt & Schiedek, 1997; Fauchald & Jumars, 1979; Ockelmann & Vahl, 1970
Prostomium shape	Small and pentagonal	Small, conical and annulate	Subtriangular	Hayward & Ryland, 2017; Scaps, 2002
Sense organs
Palps	+	+	+	Hayward & Ryland, 2017; Ravara et al., 2010
Antennae	+	+	+	Hayward & Ryland, 2017; Ravara et al., 2010
Tentacular cirri	–	–	+	Hayward & Ryland, 2017
Nuchal organs	+	+	+	Ockelmann & Vahl, 1970; Purschke, 1997; Ravara et al., 2010
Eyes	+	–	+	Hayward & Ryland, 2017; Ravara et al., 2010
Pharyngeal papillae	+	+	–	Hayward & Ryland, 2017; Ockelmann & Vahl, 1970; Ravara et al., 2010
Hard structures
Paragnaths	–	–	+, conical	Fauchald, 1977; Hayward & Ryland, 2017
Pairs of jaws	1, internal	2, perforative	1, denticulated	Dinley et al., 2010; Hayward & Ryland, 2017; Ockelmann & Vahl, 1970

Note: – absent; + present.

FIGURE 2.

The head and buccal apparatus of Nephtys hombergii. (a) Scanning electron microscopy (SEM) micrograph depicting a dorsal view of N. hombergii head and first segments (proboscis retracted). Note the small and squared prostomium (pt). (b) Stereoscopic photograph of N. hombergii head with fully everted proboscis (pb), showing the three types of papillae: subterminal (sb), middorsal (md) and terminal (tr). (c) Micrograph of the proboscis tip (SEM) with 10 pairs of soft and bifid terminal papillae (tr) surrounded by a ring of subterminal papillae (sb). (d) Detail of the bifid papillae (SEM). Scale bars: (a—c) 500 μm; (d) 200 μm.

The bloodworm G. alba exhibits a conical and annulated prostomium (Figure 3a). The relatively long proboscis of G. alba is covered with minute papillae (Figure 3b) and its tip is equipped with four smooth and delicate jaws, curved towards the mouth and with a pointed tip (Figure 3c,d), each one with a set of lined orifices that were easily visible detected by SEM analysis (Figure 3e,f). In contrast with Nepthys and Glycera, both of which bear a pair of slender antennae plus a pair of slim palps, the head region of Hediste diversicolor possesses several sensory structures, namely, a pair of articulated palps with conical palpostyles (the distal sections of the palps), where numerous sensory cilia are present (not shown). To these are added the presence of a pair of antennae on the prostomium and four pairs of tentacular cirri attached to the peristomium (Figure 4a). The proboscis of Hediste also shows a set of chitinous and conical accessory teeth (paragnaths) located on both oral and maxillary rings (the latter being the innermost ring of such structures), plus a pair of denticulated and robust jaws (Figure 4b,c). These jaws present an inward‐curved shape and a flattened surface tip (Figure 4d). In addition, unlike Nephtys and Glycera, pharyngeal papillae are absent in Hediste.

FIGURE 3.

The head, proboscis and jaws of Glycera alba. (a) Scanning electron microscopy (SEM) micrograph showing the ventral view of the conical and annulated prostomium (pt) and first segments (proboscis retracted). (b) SEM image of the prostomium (pt) lateral view with the beginning of proboscis (pb) extension and the head appendages: two dorsal antennae (an) and two ventral palps (pa). Note the numerous papillae covering the long proboscis surface. (c) SEM micrograph of the end of proboscis with four curved jaws (arrowheads). The fourth jaw is incidentally not visible. (d) Micrograph of the proboscis top perspective (SEM) showing the opening to the gut. (e) Detail on G. alba jaw showing a row of venom pores aligned (SEM). (f) Magnification of the sharp‐edged jaw with venom pores (vp) (SEM). Scale bars: (a, c, d) 400 μm; (b) 200 μm; (e, f) 50 μm.

FIGURE 4.

– The head and jaw apparatus of Hediste diversicolor. (a) Scanning electron microscopy (SEM) image of H. diversicolor prostomium composed by a pair of articulated palps (pa), a pair of antennae (an) and four small eyes (not shown). Dashed line represents the damaged antennae. Four pairs of tentacular cirri are also visible. (b) SEM micrograph of everted proboscis showing a set of chitinous accessory teeth (paragnaths, pg) and a pair of jaws (jw). (c) Higher‐power magnification of the jaw showing its denticulated inner rim to facilitate grasping and shredding (SEM). (d) Detail of the internal and smoother surface of the jaw tip (SEM). Scale bars: (a, b) 800 μm; (c) 300 μm; (d) 100 μm.

The elemental maps created by SEM–EDX analysis revealed that the jaws of Glycera and Hediste are formed by multiple elements, with emphasis on metals, in a dominant organic matrix (Figures 5 and 6, respectively). Nevertheless, the two species revealed different elemental profiles. Along the jaws of Glycera, there is a homogeneous distribution of carbon (C), oxygen (O), nitrogen (N), sulphur (S), phosphorus (P) and aluminium (Al), with higher proportions of the first three elements (Figure 5c–e, g–i). At the tip there seems to be a more conspicuous presence of copper (Cu) (Figure 5f). Contrasting to Glycera, SEM–EDX revealed that the jaw of Hediste diversicolor has a broader elemental composition, with emphasis not only on carbon, oxygen and nitrogen but also on other elements such aluminium, barium (Ba), phosphorus and sulphur, the two latest concentrated mainly at the jaw anterior part (Figure 6). Halogens such iodine (I), chlorine (Cl) are also present homogeneously along the jaw surface, whereas bromine (Br) is mostly accumulated at the tip of the jaw (Figure 6e,g,h). In spite of the relatively broad richness of elements that account for its composition, the jaws of H. diversicolor present lower levels of heavier elements (metals).

FIGURE 5.

Elemental analysis of Glycera alba jaw by scanning electron microscopy‐energy dispersive X‐ray (SEM–EDX). (a) Composite dot map of main analysed elements: aluminium (Al), nitrogen (N), oxygen (O), sulphur (S), phosphorus (P), copper (Cu) and carbon (C). (b) SEM–EDX spectra and relative percentages of the most representative elements. (c–i) Individual dot maps of C, O, N, Cu, S, P and Al, respectively.

FIGURE 6.

Elemental analysis of Hediste diversicolor jaw by scanning electron microscopy‐energy dispersive X‐ray (SEM–EDX). (a) Composite dot map of main analysed elements: carbon (C), oxygen (O), aluminium (Al), phosphorus (P), sulphur (S), chlorine (Cl), iodine (I), bromine (Br), barium (Ba), iron (Fe), silicon (Si) and fluorine (F). (b) SEM–EDX spectra and relative percentages of the most representative elements. (c–n) Individual dot maps of C, O, I, P, Cl, Br, Al, S, Fe, F, Si and Ba, respectively.

4. DISCUSSION

The jaw apparatus of the three species shows striking differences that seemingly relate to their ecology, not only with particular respect to jaw shape, size and essential composition but also concerning how the jaws are externalised and the general morphology of the prostomium.

Instead of possessing extrudable jaws, Nepthys hombergii presents one pair of delicate and inconspicuous internal jaws located within the pharynx (not shown), well described by Dinley et al. (2010). These jaws seemingly function likely a gizzard, helping to grind food particles. The different types of papillae present in the proboscis of N. hombergii are a common feature among nephtyids that may have multiple functions. In fact, several authors suggested these pharyngeal papillae have a mechanosensory role since they possess sensory cells or nerve fibres that may be responsible for full proboscis eversion when a prey is detected (Retzius, 1902; Stolte, 1932; Wallengren, 1901).

Besides feeding and sensing, locomotion is a major factor that influenced the evolution of the prostomium and proboscis in Polychaeta. In fact, it must be noted that in spite of differences in feeding behaviour, nephtyids, glycerids and nereidids are all considered efficient burrowers, but with differences in the burrowing mechanisms. Although N. hombergii is considered to be, by far, the fastest burrower, all three species rely on the rapid eversion of the muscular proboscis, in order to punch through the sediment for rapid burying (Ockelmann & Vahl, 1970; Trevor, 1976; Trevor, 1977). The presence of proboscidial papillae may also help in traction through the sediment, as described for this and other Phyllodocida (Smith et al., 1995). In turn, the conical shape of the G. alba prostomium is employed by the worm to move through sediment with a high proportion of fine particles, after the initial stage of burrowing as noted by Ockelmann and Vahl (1970). These same authors reported that this carnivorous annelid, which is an ambush predator, builds and inhabits an organised system of galleries in the sediment, inside which they sense and await potential prey. While hiding in these galleries, G. alba can perceive the mechanical stimuli caused by moving prey above as the trigger of its feeding behaviour. The authors stated that the minute papillae that cover the relatively long proboscis of G. alba could be responsible for stimuli perception, like Nephtys or even Eulalia viridis, a member of Phyllodocidae family that bears a strong and muscular proboscis entirely covered with structures that are arguably highly specialised sensory papillae, as described by Rodrigo et al. (2018). It must be noted that, besides mechanoreceptors, the papillae of glycerids host copious number of mucocytes that should allow the protection of the proboscis during burrowing and help consolidating the tubes through the formation of a soft wall made by sediment particles held together by mucus (Böggemann et al., 2000; Böggemann & Purschke, 2006). This shows that the proboscis is a multi‐purpose organ involved in burrowing, feeding, sensing and hunting, including ensnaring prey and injecting venom, as shown by the present findings The morphology of the G. alba jaws seemingly enables these polychaetes to effortlessly grab and perforate the integument of prey, making a firm grip using the hook‐shaped mandible and finally overwhelming their target by injecting venom through the jaw openings (see also Broomell et al., 2007; Michel, 1966; Ockelmann & Vahl, 1970). Studies performed by von Reumont et al. (2014), Richter et al. (2017) and Moutinho Cabral et al. (2022) have already revealed that the venom of glycerids is likely a complex mixture of proteinaceous toxins, some of which might be able of interfere with ionic channels and thus acting as neurotoxins on prey. In addition, recent toxicity testing with venomous extracts from G. alba confirmed that the proboscis is indeed the organ specialised in the secretion of toxins for predation (D'Ambrosio et al., 2022).

The diversity of sensory structures on the Hediste diversicolor head, namely, the numerous sensory cilia, may aid in food prospection, according to Fauchald and Jumars (1979). Altogether, the fact that nereidids are both active predators and deposit‐feeders is related to the structure of jaws. When Nereis is searching for food, the inward‐curved shape of the jaws allows it to seize and grasp food items and promptly ingest them or drag them to the burrow for later consumption (Evans et al., 1974; Scaps, 2002). These robust jaws are seemingly used for the shearing of food items as well. In turn, the jaws of Glycera are well‐adapted to pierce the integument of prey and enable rapid delivery of the venom.

Despite differences in their feeding behaviour, both H. diversicolor and G. alba are toxin producers; however, their noxious secretions have distinct functions and target organisms, specifically, defence and preying, respectively, which may be related to different jaw shapes. Whereas H. diversicolor secretes venomous compounds that act as protection against predators, the worms belonging to the genus Glycera specifically produce a complex cocktail, which may include neurotoxins and other bioactives with relatively precise molecular targets (Michel & Keil, 1975; von Reumont et al., 2014). These findings were also confirmed by the analysis of whole‐transcriptomes using RNA‐Seq that detected the expression of several transcripts encoding specific proteins associated with neurotoxic action in G. alba, whereas in H. diversicolor most toxin‐related transcripts were bound to defence and immune functions (see Moutinho Cabral et al., 2022). Recent work on G. alba, specifically, also showed the existence of cysteines‐bearing secreted proteins typically found in venom cocktails, highlighting its specialisation on predation, as these proteins tend to be highly reactive (D'Ambrosio et al., 2021; Gonçalves & Costa, 2020). Furthermore, the nereidid Hediste diversicolor is also able to use mucous‐devices for filter‐feeding, a behaviour that is neither described for glycerids nor nephtyids. In fact, in Hediste, a mucous net is set suspended across the temporary tubes to capture food particles that are carried through the water flow produced by the body motion of the polychaete within the tube (see for instance Goerke, 1966; Fauchald & Jumars, 1979).

Data from SEM–EDX analysis on Glycera jaws revealed the presence of copper at the tip, which is accordant with the findings of several previous authors on other species of Glycera. For instance, Gibbs and Bryan (1980), who worked on Glycera fallax (then named G. gigantea), detected high levels of copper (concentrated at the tip of the jaw) via atomic absorption analyses, which involved the digestion of different jaw sections comprising both the distal and basal halves, as well as the jaw support region. Additionally, the same authors confirmed a copper distribution pattern with X‐ray microanalysis, hitherto stating this feature to be a structural characteristic of glycerid jaws. In turn, Lichtenegger et al. (2002) using an electron microprobe analyser (EMPA) pointed out that Glycera dibranchiata jaws contain copper as copper atacamite [Cu₂(OH)₃Cl], a biomineral that may enhance hardness and stiffness. In addition, Moses et al. (2006) attributed to the organic content of Glycera dibranchiata jaws an important role in their mechanics, highlighting melanin as the responsible for chemical stability up to the point of providing the structure with exceptional resistance to both chemical and mechanical abrasion. Melanin itself has been pointed as having high affinity for metal ions such copper, thus contributing to an increase in the hardness of biological structures (Szpoganicz et al., 2002). Altogether, the jaws of Glycera, which are distinctly melanistic, possess a rather unique biometallic matrix base that holds particular importance for a delicate structure in shape that requires extra strength to pierce through skin and exoskeleton of invertebrates without significant damage.

The lower levels of heavier elements (metals) of Hediste diversicolor jaw revealed by SEM–EDX are probably associated with low melanin content, which is in accordance with previous studies that suggested that nereidids jaws are considerably less hard than those from glycerids (Birkedal et al., 2006; Lichtenegger et al., 2003; Moses et al., 2006). Although the shape and function of Glycera jaws require a particular chemical structure to ensure sufficient hardness and sharpness to perforate prey tissues, the blunt shape and large size of nereidid jaws may compensate for a weaker chemical composition. Accordingly, it has been hypothesised by Moutinho Cabral et al. (2022) that nereidids may secrete less specific, more defensive toxins compared to glycerids, therefore establishing a link between the composition and structure of the jaw apparatus in Polychaeta and the specificity of functions. It should, however, be noted that there are other important ecological factors influencing composition, such as element availability and feeding, which is more varied in nereidids. Comparatively, nephtyids like Nephtys are also opportunistic omnivores like nereidids, but with a powerful proboscis for suction instead of jaws, making them lighter and more agile epibenthic predators and foragers.

It has been noted elsewhere that estuarine Polychaeta can be particularly tolerant to pollutants, an important part of which can be related to the incorporation of metals in biominerals such as those in jaws and through the action of particular halogenase enzymes (see Coutinho et al., 2018 and Rodrigo & Costa, 2019, for review, and references therein). In the latter case, haloperoxidases have been described in several Polychaeta (e.g., Chen et al., 1991; Yoon et al., 1994), but information is lacking concerning glycerids and, moreover, nereidids, where important amounts of halogens were found in the present study. Nonetheless, the ecological role of these enzymes has not been entirely clarified and may not be restrained to detoxification. Indeed, chlorine and iodine, which were found to be evenly distributed through the Hediste jaw (together with barium), may play an important role on jaw hardening in absence of heavier metallic elements, as stated by Birkedal et al. (2006). These authors discovered that local chlorine and zinc concentrations detected in Nereis virens jaws contribute to mandibular resistance. In fact, some species are known to synthetise post‐translationally modified proteins that bear halogenated amino acid residues that harden the proteinaceous matrix. Several of these modified amino acids halogenated with chlorine, bromine and/or iodine have already been discovered in invertebrate skeletons or other hard structures (Broomell et al., 2007; Goldberg, 1976). Altogether, these findings further support the proposal that the composition and shape of the jaws in Hediste render them a blunt and robust tool for grasping and shredding, whereas in Glycera the presence of metals may enable more gracile yet sufficiently resistant jaws that act as precision‐like tools for the delivery of a venom that likely contains specific‐acting toxins. However, in either case, it is still unclear whether they reflect elemental bioavailability in their environments, despite the Polychaeta having known resilience in environments that are naturally and anthropogenically contaminated like estuaries and other transition coastal ecosystems.

5. CONCLUSIONS

Using scanning electron microscopy techniques, the present work focused on the analysis of three different predatory polychaetes and the identification of the characteristics of their jaw apparatuses. It was verified that jaw structure and shape are strongly linked with the different feeding modes, as well the ecology of each species of Polychaeta. The elemental composition revealed that mandible hardness may be dependent on the presence of specific elements in these structures such as copper and halogens as chlorine, iodine, bromine. In addition, the current findings suggest that different species of polychaetes may have different mechanisms of regulation of chemical elements present in the environment, since G. alba and H. diversicolor inhabit the same estuary and their jaws have different biomineral profiles.

AUTHOR CONTRIBUTIONS

Cátia Gonçalves performed the laboratory work and prepared the manuscript with relevant input from Pedro M. Costa. António P. Alves de Matos supported all electron microscopy analyses; Pedro M. Costa designed the experiments and supervised the work. The authors declare that there are no conflicts of interest.

Gonçalves, C. , Alves de Matos, A.P. & Costa, P.M. (2023) Comparative analysis of the jaw apparatus of three marine annelids using scanning electron microscopy: Microstructure and elemental composition. Journal of Anatomy, 243, 786–795. Available from: 10.1111/joa.13910

DATA AVAILABILITY STATEMENT

All data is provided within this research paper. Other information may be provided to readers upon request.