Secondary Seed Ingestion in Snakes: Germination Frequency and Rate, Seedling Viability, and Implications for Dispersal in Nature

The importance of vertebrate animals as seed dispersers (zoochory) has received increasing attention from researchers over the past 20 years, yet one category in particular, diploendozoochory, remains understudied. As the term implies, this is a two-phase seed dispersal system whereby a secondary seed predator (carnivorous vertebrate) consumes a primary seed predator or granivore (rodent and bird) with undamaged seeds in their digestive tract (mouth, cheek pouch, crop, stomach, or other organ), which are subsequently eliminated with feces. Surprisingly, although snakes are among the most abundant predators of granivorous vertebrates, they are the least studied group insofar as our knowledge of seed rescue and secondary dispersal in a diploendozoochorous system. Here, using live snake subjects of the Sonoran Desert (one viperid and two colubrid species) and seeds of the Foothill Palo Verde (Parkinsonia microphylla), a dominant tree of the same region, we experimentally tested germination frequency and rate, and seedling viability. Specifically, to mimic rodents with seed-laden cheek pouches, we tested whether wild-collected P. microphylla seeds placed in the abdomen of thawed laboratory mice and ingested by the snakes would retain their germination viability. Second, we examined whether seeds exposed to gut transit germinated at a greater frequency and rate than the controls. While we found strong statistical support for our first hypothesis, both aspects of the second one were not significant. Accordingly, we provide an explanation for these results based on specific life-history traits (dormant and non-dormant seeds) of P. microphylla. Our study provides support for the role of snakes as important agents of seed rescue and dispersal in nature, their potential as ecosystem engineers, and crucial evidence for the investment of field-based studies on diploendozoochorous systems in deserts and other ecosystems.

Scelidosaurus harrisonii from the Early Jurassic of Dorset, England: cranial anatomy

Scelidosaurus harrisonii is an early (Late Sinemurian) armoured ornithischian dinosaur whose remains have, to date, only been recovered from a restricted location on the south coast of Dorset (Charmouth), England. This dinosaur has been known since 1859, but only on the basis of a partial description found in two articles published in the early 1860s by Richard Owen. The original material, discovered in 1858, comprised the majority of the skull and its associated postcranial skeleton, and represents the first ever, more or less complete dinosaur discovered. In addition to the original material, a number of further discoveries have been made at Charmouth; these latter supplement the information that can be gleaned from the original specimen. This article describes the skull of Scelidosaurus. The external surface of individual skull bones in ontogenetically relatively mature individuals displays exostoses, a patina of fibrous or granular-textured bone that anchored an external shielding of keratinous scales. There is a small, edentulous rostral beak, behind which is found a row of five heterodont premaxillary teeth. There is a minimum of 22 maxillary teeth and 27 dentary teeth in jaws of the largest well-preserved individuals known to date. Both dentitions (upper and lower) are bowed medially and are sinuous longitudinally. Maxillary and dentary crowns are tilted lingually on their roots, trapezoidal in outline and have crenellate (coarsely denticulate) margins. Adjacent crowns of teeth have mesiodistally (anteroposteriorly) expanded bases that overlap slightly and are consequently arranged en echelon. The dentitions are flanked by deep cheek pouches. Tooth abrasion is usually discontinuous along the dentition. In one individual nearly all teeth seem to be fully emerged and there is little evidence of abrasion. There is no physical evidence of a predentary, but the presence of this (typically ornithischian) element may be inferred from the structure of the symphyseal region of the dentary. The external narial and antorbital fenestrae are comparatively small, whereas the orbit and temporal fenestrae are large and open. A sclerotic ring was undoubtedly present and supported the eyeball, but it is too poorly preserved to allow it to be reconstructed with accuracy. A prominent supraorbital brow ridge overhangs the orbit. There are three osteoderms: palpebral, middle supraorbital and posterior supraorbital, sutured to the dorsal margin of the orbit. The occiput provides an area for attachment of a pair of curved, keratin-sheathed, osteodermal horns. Epistyloid bones project from the ventrolateral region of the braincase; their distal ends flank the anterolateral region of the neck. Rugose facets on either side of the basioccipital are suggested to have provided attachment sites for the epistyloid bones. Internally, the skull has a deeply vaulted snout and the nasal chambers are roofed by what are here named epivomer bones that appear to have been sutured to the dorsolateral edges of the vomers. Unusually, among dinosaurs generally, an epipterygoid is preserved attached to the dorsolateral surface of the pterygoid; there is no obvious point of articulation for the epipterygoid against the lateral wall of the braincase. A deep pit on the posterior surface of the quadrate of an immature specimen is suggestive of the existence of a remnant of cranial pneumatism. This pit becomes occluded in larger, more mature specimens.

Effects of Onchung-eum, an Herbal Prescription, on 5-Fluorouracil–Induced Oral Mucositis

In most cancer patients, chemotherapy-induced oral mucositis (OM) is a frequent side effect, leading to low quality of life and delay in therapy. The aim of this study was to evaluate the effects of Onchung-eum, a well-known herbal prescription in traditional medicine comprising 8 herbs that has long been used for skin diseases, on 5-fluorouracil (5-FU)–induced OM in human pharyngeal cells and golden Syrian hamsters. DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging activity, MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay, and reactive oxygen species production were measured in vitro. The effects of Onchung-eum on OM of hamster cheek pouches induced by 5-FU were evaluated histologically and using TUNEL assay. In addition, the expression of nuclear factor-κB, caspase-3, and pro-inflammatory cytokines were measured by immunoblotting and immunohistochemistry. Significantly increased cell viability was observed in the Onchung-eum–treated groups compared with the 5-FU–treated control group. In 500 and 1000 mg/kg Onchung-eum–treated groups, the damaged epithelial layers in the cheek pouches of hamsters were significantly recovered. Moreover, at all concentrations, cell death in the cheek pouches of hamsters in the Onchung-eum–treated groups significantly decreased. The expression of pro-inflammatory cytokines, nuclear factor-κB, and caspase-3 also significantly decreased in Onchung-eum–treated groups at 500 and 1000 mg/kg. In conclusion, this study revealed that Onchung-eum can be used to treat chemotherapy-induced OM. However, further studies are required to understand the underlying mechanisms.

Divergent Behavior Amid Convergent Evolution: A Case of Four Desert Rodents Learning to Respond to Known and Novel Vipers

ABSTRACTDesert communities word-wide are used as natural laboratories for the study of convergent evolution, yet inferences drawn from such studies are necessarily indirect. Here, we brought desert organisms together (rodents and vipers) from two deserts (Mojave and Negev). Both predators and prey in the Mojave have adaptations that give them competitive advantage compared to their middle-eastern counterparts. Heteromyid rodents, kangaroo rats and pocket mice, have fur-lined cheek pouches that allow the rodents to carry larger loads under predation risk compared to gerbilline rodents. Sidewinder rattlesnakes have heat-sensing pits, allowing them to hunt better on moonless nights when their Negev sidewinding counterpart, the Saharan horned vipers, are visually impaired. In behavioral-assays, we used giving-up density (GUD) to gage how each species of rodent perceived risk posed by known and novel snakes. We repeated this for the same set of rodents at first encounter and again two months later following intensive “natural” exposure to both snake species. Pre-exposure, all rodents identified their evolutionarily familiar snake as a greater risk than the novel one. However, post-exposure all identified the heat-sensing sidewinder rattlesnake as a greater risk. The heteromyids were more likely to avoid encounters with, and discern the behavioral difference among, snakes than their gerbilline counterparts.

Seed ingestion and germination in rattlesnakes: overlooked agents of rescue and secondary dispersal

Seed dispersal is a key evolutionary process and a central theme in the population ecology of terrestrial plants. The primary producers of most land-based ecosystems are propagated by and maintained through various mechanisms of seed dispersal that involve both abiotic and biotic modes of transportation. By far the most common biotic seed transport mechanism is zoochory, whereby seeds, or fruits containing them, are dispersed through the activities of animals. Rodents are one group of mammals that commonly prey on seeds (granivores) and play a critical, often destructive, role in primary dispersal and the dynamics of plant communities. In North America, geomyid, heteromyid and some sciurid rodents have specialized cheek pouches for transporting seeds from plant source to larder, where they are often eliminated from the pool of plant propagules by consumption. These seed-laden rodents are commonly consumed by snakes as they forage, but unlike raptors, coyotes, bobcats, and other endothermic predators which eat rodents and are known or implicated to be secondary seed dispersers, the role of snakes in seed dispersal remains unexplored. Here, using museum-preserved specimens, we show that in nature three desert-dwelling rattlesnake species consumed heteromyids with seeds in their cheek pouches. By examining the entire gut we discovered, furthermore, that secondarily ingested seeds can germinate in rattlesnake colons. In terms of secondary dispersal, rattlesnakes are best described as diplochorous. Because seed rescue and secondary dispersal in snakes has yet to be investigated, and because numerous other snake species consume granivorous and frugivorous birds and mammals, our observations offer direction for further empirical studies of this unusual but potentially important channel for seed dispersal.

The productivity of the macroinvertebrate prey of the platypus in the upper Shoalhaven River, New South Wales

The platypus (Ornithorhynchus anatinus) feeds almost exclusively on benthic macroinvertebrates, yet no attempt has been made to link its energy demands with the productivity of its benthic macroinvertebrate prey. In the upper Shoalhaven River, New South Wales, we estimated macroinvertebrate production (in 2009 and 2011) from benthic samples and recorded platypus diet (2009 only) from cheek pouch samples. Ephemeroptera, Trichoptera and Chironomidae were the most numerous of six major groups in both the cheek pouches and the benthic samples. Three other groups (Odonata, Coleoptera, Sphaeriidae) were much less abundant in the benthos, but Odonata were common in the cheek pouches. In both years the Ephemeroptera, Trichoptera and Chironomidae had levels of production that were an order of magnitude higher than those of the three other groups. Rank correlation indicated that the most productive taxa were those most likely to occur in the cheek pouches. Total macroinvertebrate production for the six groups varied from 7.8gDWm–2year–1 in 2009 to 13.1gDWm–2year–1 in 2011. Previous estimates of field metabolic demand of the platypus enabled calculation of the number that could be supported by a given level of production. The observed levels of production were sufficient to support 13–27 platypuses in 2009 and 22–45 in 2011 along a 1.5-km reach of the river. Despite considerable landscape change, productive foraging habitat persists in the upper Shoalhaven River.