Content uploaded by Vladimir Malakhov
Author content
All content in this area was uploaded by Vladimir Malakhov on Oct 03, 2015
Content may be subject to copyright.
A preview of the PDF is not available
The First Finding of a Sea Spider (Pantopoda) Planktonic Larva
... femoratum kept in the laboratory, and this allowed us to reliably identify the larva found in the plankton sample as Phoxichilidium femoratum (Rathke 1799). As far as we know, it is the first reported finding of a sea spider larva in plankton (Malakhov and Bogomolova, 2001). Morphological features of Ph. femoratum larvae suggest that this finding is not purely accidental. ...
... The small size of Ph. femoratum larvae facilitates their floating in the water and gives them the capability of pelagic dispersal, while high fertility together with small egg size counterbalances the high probability of larval death during their planktonic existence and after unsuccessful attempts to invade the host. Unusually long third segments of larval legs facilitating floating in water (Malakhov and Bogomolova, 2001) may be an additional adaptation to pelagic dispersal. Dogiel (1913), describing the development of Anoplactylus pygmaeus (Hodge 1864), also belonging to Phoxichiliidae family, mentioned that though endoparasitic development is characteristic of this species, 5-10% of larvae undergo "metamorphosis" sitting on the outer surface of the polyp. ...
The postembryonic development of five pycnogonid species from the White Sea is described. Three types of their development are specified. The first type is characterized by the development of six-legged (protonymphon) larvae of medium size (120-220 μm). They develop on ovigerous legs of males for some time, and then parasitize on hydrozoan polyps. The second developmental type is characterized by small-sized (about 50 μm) protonymphon larvae. Six-legged larvae of Phoxichilidium femoratum have some adaptations for pelagic circulation. Afterwards, they are endoparasites. Pycnogonids with postembryonic development of the third type have no typical protonymphon larvae. Large larvae of the third type are of about 300-700 μm long and with a high yolk reserve. They remain on egg cocoons carred by male on its ovigerous legs until the development of abdomen and three or four pairs of walking legs and then leave the male. Some morphological features of larvae are discussed depending on a type of development.
... The three-articled structure of their larval legs is maintained, but the terminal claw is lengthened, sometimes extremely so. Malakhov and Bogomolova (2001) proposed that elongated claws aid in dispersal. Indeed, the larvae of, for example, Phoxichilidium femoratum never linger with the parent (the egg package may start to disintegrate before hatching, personal observations), but neither do they need active locomotion after entering the host's gut. ...
Nymphon grossipes is a common subtidal species belonging to a small and unique group of chelicerates, i.e., the sea spiders. These animals have an anamorphic phase during post-embryonic development and often hatch as small, oligomeric and exotrophic larvae (protonymphons) with four postocular segments, cheliphores and two pairs of larval legs. A common alternative to protonymphons is a large lecithotrophic larval type, where animals hatch at more advanced stages and have a foreshortened anamorphic development. Based on external morphology, N. grossipes was believed to be an intriguing intermediate between these two conditions and its hatchlings were called ‘lecithotrophic protonymphons’. Here, we examine the anatomy and ultrastructure of instars I and II and review the variety of roles of larval appendages and associated glands in other sea spiders in order to correctly place the larva of this species among pycnogonid larval types. Compared to ‘typical protonymphons’, N. grossipes young hatch with an advanced segmental and appendage composition: six postocular segments instead of four, buds of walking legs 1 and hidden buds of walking legs 2. This state corresponds to the instars II/III (rather than larvae) of Nymphon brevirostre and Pycnogonum litorale. Modifications of the larval appendages, chelar and spinning glands are aligned with ecological needs of different larval types along a few typical dimensions: locomotion and feeding, dispersal, and attachment to the parent. Although the main challenge for N. grossipes young is secure attachment to the egg package while they growth, there are some discrepancies in their anatomy: N. grossipes retains an oyster basket, but an otherwise non-functional digestive system, and a strong silken thread for attachment, but no corresponding reduction of the larval legs. Thus, it is likely that the switch to lecithotrophy happened in the recent evolutionary history of this species.
... Finally, very few records are from plankton samples (e.g. Propallene longiceps (Böhm, 1879), see Utinomi (1959) or protonymphon of Phoxichilidium femoratum (Rathke, 1799), see Malakhov and Bogomolova (2001)). ...
... On the other hand, the small type 1 protonymphon larva of other pallenopsids [29,30] implies its early abandonment of the father followed by anamorphic development on/in an invertebrate host. While most type 1 protonymphon larvae do not show specific structural adaptations that may facilitate floating and dispersal in open water, exceptions are known in the form of flagelliform distal limb extensions or lamellae/dense setae fields on larval limb articles [45,[50][51][52]. Even without specialized structures, larval dispersal via open water has been suggested based on the observation that hosts infested with larvae of a species were frequently devoid of the respective adults (e.g., [53] for Endeis spinosa). ...
Background
Sea spiders (Pycnogonida) are an abundant faunal element of the Southern Ocean (SO). Several recent phylogeographical studies focused on the remarkably diverse SO pycnogonid fauna, resulting in the identification of new species in previously ill-defined species complexes, insights into their genetic population substructures, and hypotheses on glacial refugia and recolonization events after the last ice age. However, knowledge on the life history of many SO pycnogonids is fragmentary, and early ontogenetic stages often remain poorly documented. This impedes assessing the impact of different developmental pathways on pycnogonid dispersal and distributions and also hinders pycnogonid-wide comparison of developmental features from a phylogenetic-evolutionary angle.
Results
Using scanning electron microscopy (SEM) and fluorescent nuclear staining, we studied embryonic stages and postembryonic instars of three SO representatives of the taxon Pallenopsidae (Pallenopsis villosa, P. hodgsoni, P. vanhoeffeni), the development of which being largely unknown. The eggs are large and yolk-rich, and the hatching stage is an advanced lecithotrophic instar that stays attached to the father for additional molts. The first free-living instar is deduced to possess at least three functional walking leg pairs. Despite gross morphological similarities between the congeners, each instar can be reliably assigned to a species based on body size, shape of ocular tubercle and proboscis, structure of the attachment gland processes, and seta patterns on cheliphore and walking legs.
Conclusions
We encourage combination of SEM with fluorescent markers in developmental studies on ethanol-preserved and/or long term-stored pycnogonid material, as this reveals internal differentiation processes in addition to external morphology. Using this approach, we describe the first known cases of pallenopsid development with epimorphic tendencies, which stand in contrast to the small hatching larvae in other Pallenopsidae. Evaluation against current phylogenetic hypotheses indicates multiple gains of epimorphic development within Pycnogonida. Further, we suggest that the type of development may impact pycnogonid distribution ranges, since free-living larvae potentially have a better dispersal capability than lecithotrophic attaching instars. Finally, we discuss the bearing of pycnogonid cheliphore development on the evolution of the raptorial first limb pair in Chelicerata and support a multi-articled adult limb as the plesiomorphic state of the chelicerate crown group, arising ontogenetically via postembryonic segmentation of a three-articled embryonic limb.
Electronic supplementary material
The online version of this article (10.1186/s40851-018-0118-7) contains supplementary material, which is available to authorized users.
... The males carry the offspring from the eggs to first protonymphon larva stage on specialised appendages, the ovigera. In contrast to many other marine invertebrates that have an obligatory pelagobenthic life-cycle with larvae going through a planktonic dispersal phase, in sea spiders the dispersal of single individuals over long distances has been suggested to be an occasional rather than a regular element of the life-cycle (observations for adult pycnogonids, e.g. in Pagès et al. 2007;and for protonymhons in Bain 2003;Malakhov and Bogomolova 2001). Though it is the earliest stage of many pycnognonids, the protonymphon larva can be harvested directly from the egg packages on the ovigers of their fathers, and therefore can easily be attributed to a distinct species; however, detailed descriptions of protonymphon larvae are available for onlỹ 5% of the species (Fornshell 2014). ...
We used scanning electron microscopy (SEM) to establish species-specific sets of characters for protonymphon larvae of two representatives of the 'patagonica' species group of Pallenopsis, P. patagonica and P. yepayekae. The larvae of both species are 'typical' protonymphon larvae sensu Bain (2003). Despite the close relationship of the two species, we observed numerous features that allow for differential diagnosis, e.g. general habitus, the number, arrangement and branching type of setules, the armature of the movable and immovable chelifore fingers, and the shape of the dactylus and setules of appendages II and III. SEM is particularly suitable for visualising these features. Our results further support the idea that protonymphon larvae can be identified to species level when adequate imaging techniques are used, as is also the case for larvae of other arthropods. Moreover, the status of the two studied species of Pallenopsis is fully supported by protonymphon larval morphology.
... The larval proboscis is very prominent and the larval cheliphores lack the attachment gland and its spine. The terminal articles of the palpal and ovigeral larval limbs are elongated and filamentous, which may facilitate locomotion ("walking") over benthic communities and/or floating and dispersal in the pelagic zone, as suggested by larvae of Phoxichilidium femoratum found in plankton samples [83]. They are also used to hold on to the host [38]. ...
Background:
Arthropod diversity is unparalleled in the animal kingdom. The study of ontogeny is pivotal to understand which developmental processes underlie the incredible morphological disparity of arthropods and thus to eventually unravel evolutionary transformations leading to their success. Work on laboratory model organisms has yielded in-depth data on numerous developmental mechanisms in arthropods. Yet, although the range of studied taxa has increased noticeably since the advent of comparative evolutionary developmental biology (evo-devo), several smaller groups remain understudied. This includes the bizarre Pycnogonida (sea spiders) or "no-bodies", a taxon occupying a crucial phylogenetic position for the interpretation of arthropod development and evolution.
Results:
Pycnogonid development is variable at familial and generic levels and sometimes even congeneric species exhibit different developmental modes. Here, we summarize the available data since the late 19(th) century. We clarify and resolve terminological issues persisting in the pycnogonid literature and distinguish five developmental pathways, based on (1) type of the hatching stage, (2) developmental-morphological features during postembryonic development and (3) selected life history characteristics. Based on phylogenetic analyses and the fossil record, we discuss plausible plesiomorphic features of pycnogonid development that allow comparison to other arthropods. These features include (1) a holoblastic, irregular cleavage with equal-sized blastomeres, (2) initiation of gastrulation by a single bottle-shaped cell, (3) the lack of a morphologically distinct germ band during embryogenesis, (4) a parasitic free-living protonymphon larva as hatching stage and (5) a hemianamorphic development during the postlarval and juvenile phases. Further, we propose evolutionary developmental trajectories within crown-group Pycnogonida.
Conclusions:
A resurgence of studies on pycnogonid postembryonic development has provided various new insights in the last decades. However, the scarcity of modern-day embryonic data - including the virtual lack of gene expression and functional studies - needs to be addressed in future investigations to strengthen comparisons to other arthropods and arthropod outgroups in the framework of evo-devo. Our review may serve as a basis for an informed choice of target species for such studies, which will not only shed light on chelicerate development and evolution but furthermore hold the potential to contribute important insights into the anamorphic development of the arthropod ancestor.
... Introducing a plankton net, possibly at night with a light, in shallow and deep waters might be a method that would reveal new or rare species along the Norwegian coast. The first record of a planktonic larva of a sea spider was also made using a plankton net (Malakhov & Bogomolova 2001). ...
Knowledge of sea spider (Pycnogonida, Arthropoda) distribution and habitat preferences within Norwegian waters is scarce. During the MAREANO programme from 2007 to 2009, 3909 pycnogonid specimens representing 21 species and nine genera were collected. Pycnogonida were found at a total of 60 stations from 78 to 2609 m depth using van Veen grab, RP-sledge and beam trawl. Nymphon, the dominant genus, constituted 52% of the specimens sampled. Cilunculus battenae was recorded for the first time within Norwegian waters, and Pseudopallene longicollis was recorded for the first time in Norwegian
Arctic waters (72°16′N, 14°36′E at ‒0.64°C). New records of Pseudopallene brevicollis, Boreonymphon robustum and B. ossiansarsi were made. Boreonymphon abyssorum and Nymphon macronyx showed the widest depth ranges (100–2000 m depth). The known northern distribution of Callipallene producta was extended to 71°42′N, 15°25′E, Northern Norway. Two-thirds of the species found had their centre of distribution below 500 m and a species diversity maximum was found at 800–900 m. Four main species groups with different depth distributions were identified by cluster analysis: (1) shallow, above transition zone; (2) lower part of transition zone; (3) lower transition zone, wide ranging; and (4) mainly below 1000 m depth. A Detrended Correspondence Analysis supported the same pattern of clustering.
... A summary of earlier literature of larval development of different species is also given in Bain (2003a). In addition, the postembryonic development was studied, e.g. in Nymphon distensum Möbius, 1902in Munilla (1988; Phoxichilidium femoratum (Rathke, 1799) in Malakhov & Bogomolova (2001); Austropallene cornigera (Möbius, 1902) in Bain (2003b); Tanystylum bealensis Gillespie & Bain, 2005in Gillespie & Bain (2006; Phoxichilidium femoratum (Rathke, 1799) in Lovely (2005); Nymphon grossipes Kroyer, 1845 in Bogomolova & Malakhov (2006); Nymphon brevirostre Hodge, 1863, Nymphon micronyx Sars, 1888, and Nymphon grossipes Fabricius, 1780 in Bogomolova (2007); and Ammothea glacialis (Hodgson, 1907) in Cano & Lopez-Gonzalez (2009). In the latter, description of the protonymphon is missing. ...
The present paper is the first scanning electron microscope (SEM) description of a protonymphon larva of an Ammotheidae. The morphology of the first larval instar of Achelia assimilis is described in detail and illustrated for the first time. The morphological characters are compared to previous larval descriptions of other pycnogonid species. The larvae are integrated into Bain's classification of larval types within the pycnogonids (Bain, 2003a) as a ‘typical protonymphon’. Larvae were obtained from ovigerous males, caught in Punta Huinay, Huinay, Chile and analysed with light microscope and SEM. Descriptions of pycnogonid protonymphons at a species-specific level in the future will contribute to a deeper understanding of larval pycnogonid taxonomy at the level of differential diagnoses.
... For instance, only species shown to have an 'encysting' development have larvae with modified terminal articles: in the place of claws they have long filamentous strands up to five times the length of their bodies (Hilton, 1916;Lebour, 1945;Bain, 2003;Lovely 2005). A larva with characteristics of the encysting mode of development has been found in the plankton, making it possible that these long strands are an adaptation to the pelagic environment by decreasing the rate of larval sinking (Malakhov & Bogomolova, 2001). They may also be provisional structures for movement to the larva's hydroid host (Russel, 1990;Lovely, 2005). ...
Larvae of eight sea spiders from three families (Ammotheidae, Pycnogonidae and Phoxichilidiidae) are described for the first time. The external morphology of the first larval stage of each species is presented in detail using scanning electron microscopy photographs in order to determine the mode of postembryonic development. Three types of larval development are apparent in the species examined. The species Achelia gracilipes, Eurycyde spinosa, Pycnogonum rickettsi and Pycnogonum stearnsi (families Ammotheidae and Pycnogonidae) have larval morphologies indicative of an ‘ectoparasitic’ development. Morphological characteristics of Achelia simplissima and Achelia chelata (family Ammotheidae) larvae suggest an ‘endoparasitic’ development, while larvae of the species Anoplodactylus viridintestinalis (family Phoxichilidiidae) have traits implying an ‘encysting’ postembryonic mode of development. Larvae of the species Nymphopsis spinosissima have unusual morphological characteristics that may be indicative of a new developmental mode.
Phoxichilidium tubulariae exhibits an encysted protonymphon development. Its fast developmental mode reduced the typical number of pycnogonid molts and developmental time from months as described for other pycnogonid species to fewer than 21 days. This developmental strategy exploited the seasonal abundance of Tubularia larynx. The larvae hatched, infested the hydroid, and developed inside the gastrovascular cavity. The larvae developed for several molts and then emerged, destroying the hydranth. Annual population dynamics of P. tubulariae were seasonal; density of adult animals was highest in mid-to-late summer with reproduction being greatest in July and August. The abundance of pycnogonids peaked as the hydroid population declined.
ResearchGate has not been able to resolve any references for this publication.