Tasmanian Cave Research Articles

Hooroo mates! Phylogenomic data suggest that the closest relatives of the iconic Tasmanian cave spider Hickmania troglodytes are in Australia and New Zealand, not in South America

Hickmania troglodytes is an emblematic cave spider representing a monotypic cribellate spider genus. This is the only Australian lineage of Austrochilidae while the other members of the family are found in southern South America. In addition to being the largest spider in Tasmania, Hickmania is an oddity in Austrochilidae because this is the only lineage in the family bearing posterior book lungs, tarsal spines and an embolar process on male pedipalps. Six-gene Sanger sequences and genome scale data such as ultraconserved elements (UCEs) and transcriptomes have suggested that Hickmania troglodytes is not nested with the family of current classification, Austrochilidae. We studied the phylogenetic placement of Hickmania troglodytes using an increased taxon sample by combining publicly available UCE and UCEs recovered from transcriptomic data in a parsimony and maximum likelihood framework. Based on our phylogenetic results we formally transfer Hickmania troglodytes from Austrochilidae to the family Gradungulidae. The cladistic placement of Hickmania in the family Gradungulidae fits the geographic distribution of both gradungulids (restricted to Australia and New Zealand) and austrochilids (restricted to southern South America) more appropriately.

The biomimetics potential of cave-dwelling animals

Biomimetics or biologically inspired design is a relatively new interdisciplinary field that aims to harness the processes and mechanisms in nature that have been optimised over million of years’ evolution to improve our own technology. There are two main approaches to biological inspired design – the problem-driven approach starting with an engineering problem and searching through biological equivalents or the solution-driven approach which starts with a biological example or solution followed by the identification of a suitable engineering application (Lenau et al. 2018). While the former approach is the most popular and is favoured by engineers, the latter remains the most successful and is typically driven by fundamental biological research. However, no biomimetic solutions or concepts have so far been described from subterranean habitats despite the rich potential arising from the wonderfully diverse range of bizarre morphological, physiological and behavioural adaptations that have arisen in response to the environmental constraints. In this presentation I give an outline of potential biomimetics examples arising from cave-dwelling animals in three technology fields. Biomaterials – the high humidity, lack of light and stable temperatures may have given rise to novel biomatarials. A promising study on the properties of silk from the Tasmanian cave spider Hickmania troglodytes is currently underway (Piorkowski et al. 2017). Adhesion devices. The high humidity and smooth wet surfaces underground may have given rise to unique morphological adaptations to adhere to and move on these surfaces. Potential target organisms include millipedes, springtails and cave angel fish. Biorobotics. Biomaterials – the high humidity, lack of light and stable temperatures may have given rise to novel biomatarials. A promising study on the properties of silk from the Tasmanian cave spider Hickmania troglodytes is currently underway (Piorkowski et al. 2017). Adhesion devices. The high humidity and smooth wet surfaces underground may have given rise to unique morphological adaptations to adhere to and move on these surfaces. Potential target organisms include millipedes, springtails and cave angel fish. Biorobotics. The characteristics of the subterranean habitats potentially offer rich inspiration for the design of exploration robots ranging from flexible movement in constrained spaces, flight in low light conditions and non-visual navigation. The hope is that this presentation will inspire experienced biospeleologists to consider and explore potential novel biomimetic applications in their own study organisms.

Web-building behavior of the odd-clawed spider Progradungula otwayensis (Araneae: Gradungulidae) and implications for the evolution of combing behavior in spiders

This study explores the web-building behavior of Gradungulidae for the first time, using the Otway odd-clawed spider Progradungula otwayensisMilledge, 1997. The web consists of a signal line leading to a retreat, an upper scaffold and a cribellate catching ladder connected to the substrate. The construction sequence and final structure of the catching ladder are highly stereotyped, especially in the initial segments of the cribellate capture thread. Two vertical rail lines—made of thin cribellate silk that is not combed with the calamistrum—are connected by looping segments of combed, much thicker cribellate capture threads. Small juveniles make a relatively larger non-sticky supporting scaffold with some cribellate silk on it. Microscopic analysis of the silk revealed that the cribellate bands have a pair of axial lines and a pair of reserve warps; the cribellate fibrils have nodules. The non-sticky structural lines are made of straight or coiling lines, changing gradually from straight to coiling; each of these structural lines is composed of tightly appressed fibrils, probably associated with the occurrence of multiple ampullate gland spigots. During combing behavior both legs IV are used synchronously. The same combing behavior is performed by the Tasmanian cave spider Hickmania troglodytes (Higgins & Petterd, 1883). We conclude that both type I and type II combing behaviors are monophyletic, although it is unclear which one is ancestral. Given the phylogenetic position of ProgradungulaForster & Gray, 1979, we suggest that the ability to measure with precision and produce repetitive, stereotyped silk structures made of specific silk types may have arisen close to the ancestor of araneomorph spiders.

Ontogenetic shift toward stronger, tougher silk of a web‐building, cave‐dwelling spider

AbstractAnimal morphological traits may vary across life stages. Web‐building spiders are diverse insectivores that can display ontogenetic shifts in the design and properties of their webs. Nevertheless, we know little about how a critical component of their webs, major ampullate silk (MAS), varies in property across life stages, inferably owing to a difficulty in finding suitable model species. The Tasmanian cave spider Hickmania troglodytes presents as a good model as it is long‐lived and grows to a large body size with overlapping generations. We collected MAS from the webs of different‐sized H. troglodytes and performed tensile tests on MAS fibers collected from their webs to search for shifts in properties over life stages. We found that strength and toughness (i.e. ability to deform and absorb energy) of the MAS increased with spider carapace width and body length. We expect that such a shift in silk performance across life stages has distinctive advantages, including enhanced prey capture capabilities, an improvement in the economy of silk production and ability of the web to support the spider's larger body.

Morphological evidence for limited sperm production in the enigmatic Tasmanian cave spider Hickmania troglodytes (Austrochilidae, Araneae)

AbstractThe male reproductive systems of spiders are highly diverse in structure across all major spider taxa. Little is known about this organ system in basal araneomorph spiders, especially Austrochiloidea; such knowledge is necessary for a more complete understanding of the evolutionary morphology of the male reproductive system in spiders. In the present study, we describe the male reproductive system of an austrochilid spider, the enigmatic troglophilic Tasmanian cave spider Hickmania troglodytes, using light and electron microscopic techniques. The male reproductive system consists of tubular testes leading into convoluted deferent ducts, which are fused close to the genital opening to an unpaired ejaculatory duct. Spermatogenesis occurs only in the subadult testes, whereas adult testes showed neither spermatogenic stages nor any generative tissue in all investigated specimens. The testes of adult males are drastically reduced in size compared with those of subadult males, but the deferent ducts are filled with large numbers of mature spermatozoa. Thus, our data suggest that males of H. troglodytes are sperm‐limited, but not necessarily sperm‐depleted as described for certain orb‐weaving spiders. Due to the absence of generative tissue, limited sperm production is permanent (PSL) and probably has an influence on the reproductive strategies in this species. As nearly no data are available on the life history of H. troglodytes, and in particular information on the phenology of males is lacking, implications of the evolution of PSL in this species are unclear. Nonetheless, our data on other representatives of Austrochilidae (Austrochilus forsteri, Thaida chepu) and Gradungulidae (Progradungula otwayensis) suggest that PSL evolved within Austrochiliodea only in H. troglodytes and might be an adaptation to its troglophilic lifestyle.

Overdone overkill – the archaeological perspective on Tasmanian megafaunal extinctions

The reasons for megafaunal extinction in Australia have been hotly debated for over 30 years without any clear resolution. The proposed causes include human overkill, climate, anthropogenic induced habitat change or a combination of these. Most protagonists of the human overkill model suggest the impact was so swift, occurring within a few thousand years of human occupation of the continent, that archaeological evidence should be rare or non-existent. In Tasmania the presence of extinct megafauna has been known since the early twentieth century ( Noetling, 1912; Scott, 1911, 1915) with earlier claims of human overlap being rejected because of poor chronology and equivocal stratigraphic associations. More recent archaeological research has not identified any megafauna from the earliest, exceptionally well-preserved late Pleistocene cultural sites. In 2008 however an argument for human induced megafaunal extinctions was proposed using the direct dates from a small sample of surface bone from two Tasmanian non-human caves and a museum sediment sample from an unknown location in a cave, since destroyed by quarrying ( Turney et al., 2008). Turney et al. (2008) supplemented their data with published dates from other Tasmanian caves and open sites to argue for the survival of at least seven megafauna species from the last interglacial to the subsequent glacial stage. To investigate the timing of extinctions in Tasmania and examine the latest claims, new excavations and systematic surveys of limestone caves in south central Tasmania were undertaken. Our project failed to show any clear archaeological overlap of humans and megafauna but demonstrated that vigilance is needed when claiming survival of megafauna species based on old or suspect chronologies. The results of our six-years of fieldwork and dating form the first part of the present paper while, in the second part we assess the data advanced by Turney et al. (2008) for the late survival of seven megafauna species. A model of human prey selection and the reasons for the demise of a range of marsupials, now extinct, are discussed in the third part of the paper.

Systematic seasonal land use by late Pleistocene Tasmanian Aborigines

New research on the odontochronological (dental growth-increment) analysis of marsupial teeth provides opportunities to estimate with more certainty the time of the year Tasmanian Aborigines inhabited sites during the late Pleistocene. Here we focus on the Bennett's wallaby ( Macropus rufogriseus) as a proxy for understanding seasonal human land use patterns and occupation of four southwest Tasmanian caves. The aim of the paper is to investigate whether caves at different altitudes were occupied in alternating seasons, and determine if the ‘Patch Model’ developed to explain the archaeological variability of late Pleistocene human behavior should be modified accordingly. The data presented here support the original observations that these sites, although reflecting extreme richness, were occupied in a punctuated seasonal manner with visits probably separated by a considerable time of unknown duration.

The reproductive behaviour of the Tasmanian cave spider Hickmania troglodytes (Araneae: Austrochilidae)

Abstract Hickmania troglodytes, the Tasmanian cave spider, belongs to a relict group with a scattered world distribution, and is of both phylogenetic and zoogeographic interest. It belongs to the superfamily Austrochiloidea (infra‐order Araneomorphae) and shares characteristics with more advanced araneomorphs and primitive spiders in the infra‐orders Liphistiomorphae and Mygalomorphae. The reproductive behaviour of H. troglodytes (including courtship, mating, egg‐sac construction, brooding, emergence, and moulting behaviour) is described, providing the first such account for any member of the Austrochiloidea. Courtship in H. troglodytes is ritualized and involves distinct communicatory gestures (beating with the legs) by the male to identify and protect himself. Males use a pronounced curve in the metatarsus of the second leg to immobilize females during mating; this curve closely matches the contours of the female's cheliceral region. Both courtship and mating are protracted and each can last for over 5.5 h. The egg‐sac is large and unusual, with a rigid internal structure that separates the egg mass from the silk walls, while the silk itself seems to be exceptionally resistant to fungal degradation. The young emerge from the egg‐sac 8–10 months after laying, a period significantly longer than the typical emergence time of araneomorph spiders (4–8 weeks). It is suggested that the rigid internal structure and the silk of the egg‐sacs may help to buffer and protect the eggs and young from biotic and abiotic factors during this extended pre‐emergence period.

Hickmania troglodytes, the Tasmanian cave spider, and its potential role in cave management

Cave faunas – which often contain a high representation of spiders – are subject to increasing pressure from the effects of epigean habitat degradation and recreational caving activities. Hickmania troglodytes is a prominent member of the Tasmanian cave fauna, a spider of phylogenetic, zoogeographic and ecological importance, but about which little has previously been known. Long-term monitoring has revealed many unusual life-cycle characteristics in this species, most of which occur over long periods of time and are dependent upon environmental stability. The species presents a potentially useful tool in the management and monitoring of cave fauna and karst, as it is large, conspicuous, numerous, ubiquitous, sedentary, functionally significant and potentially sensitive to various sources of disturbance. H. troglodytes may provide a visible and obvious measure of disturbance in and around cave entrances, and may also prove useful in detecting broader scale impacts affecting the entire cave. Many promising developments are being made in terms of cave management in Tasmania, but other issues are less well addressed and still need to be resolved. With further research, the use of indicator or sentinel species may prove to be well suited to the less complex and often sparsely populated subterranean environment, and may play an important role within larger management strategies for cave fauna and karst.

Invertebrate biodiversity and conservation in Tasmanian caves

Invertebrate biodiversity and conservation in Tasmanian caves

A New Troglobitic Species of Hanseniella Bagnall (Symphyla: Scutigerellidae) from Tasmania

ABSTRACTA new species of Symphyla, Hanseniella magna, is described from two Tasmanian caves. It is the largest symphylan ever collected and has exceptionally elongate antennae, claws and cerci.

Late Pleistocene palaeotemperature record from a Tasmanian speleothem

Multiple 230Th/234U age determinations on a uniform diameter calcite stalagmite from a Tasmanian cave show that it was deposited between 109 000 and 76 000 years BP at a constant rate of 4.3 cm per 100 years. Except for the first 9000 years, deposition occurred under conditions of oxygen isotope equilibrium enabling it to be used for palaeotemperature studies. Measurements of 18O/16O ratios of calcite and d/h ratios of fluid inclusions indicate that mean annual temperatures at the site were nearly always lower than at present from 100 000 to 76 000 BP. A positive relationship is found between mean annual temperature and the 18O/16O content of calcite. This is uncommon and represents the first such relationship recorded from the Southern Hemisphere. The stalagmite shows evidence of having grown during two distinct temperature phases. From 100 000 to 97 000 years BP mean annual temperatures were between 4°C and 6°C compared with a present day value of 9.5°C. At about 97 000 years BP there was a rapid transi...

Electron spin resonance dating of Quaternary bone material from Tasmanian caves—A comparison with ages determined by aspartic acid racemization and C14

Abstract Fourteen bone samples are analysed to test the usefulness of equivalent dose (ED) determinations by electron spin resonance (ESR) as a rapid method of determining relative age and making an estimate of absolute age. ED values are compared with eight aspartic acid dates and two C14 dates. The latter are dates on charcoal found in close association with bone at archaeological sites. For samples less than 25 000 years old an excellent correlation is obtained when ED values are compared with dates obtained by the other two methods. The relationship suggests that ED values can be converted to estimates of bone age by assuming a mean annual dose rate of 0.1 rad/yr. Age determinations provide little evidence to support earlier suggestions that elements of the Late Pleistocene megafauna survived until the end of the Pleistocene. Bone material at some sites in the‐Florentine Valley and near Montagu appears to be much older than had previously been believed. Only one site (Main Cave, Montagu) containing me...