Elena Macías-Sánchez

Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism

One of the most important defensive host traits against brood parasitism is the detection and ejection of parasitic eggs from their nests. Here, we explore the possible role of olfaction in this defensive behaviour. We performed egg‐recognition tests in magpie Pica pica nests with model eggs resembling those of parasitic great spotted cuckoos Clamator glandarius. In one of the experiment, experimental model eggs were exposed to strong or moderate smell of tobacco smoke, whereas those of a third group (control) were cleaned with disinfecting wipes and kept in boxes containing odourless cotton. Results showed that model eggs with strong tobacco scent were more frequently ejected compared with control ones. In another experiment, models were smeared with scents from cloacal wash from magpies (control), cloacal wash or uropygial secretions from cuckoos, or human scents. This experiment resulted in a statistically significant effect of treatment in unparasitized magpie nests in which control model eggs handled by humans were more often rejected. These results provide the first evidence that hosts of brood parasites use their olfactory ability to detect and eject foreign eggs from their nests. These findings may have important consequences for handling procedures of experimental eggs used in egg‐recognition tests, in addition to our understanding of interactions between brood parasites and their hosts.

Crystallographic control on the substructure of nacre tablets

Nacre tablets of mollusks develop two kinds of features when either the calcium carbonate or the organic portions are removed: (1) parallel lineations (vermiculations) formed by elongated carbonate rods, and (2) hourglass patterns, which appear in high relief when etched or in low relief if bleached. In untreated tablets, SEM and AFM data show that vermiculations correspond to aligned and fused aragonite nanogloblules, which are partly surrounded by thin organic pellicles. EBSD mapping of the surfaces of tablets indicates that the vermiculations are invariably parallel to the crystallographic a-axis of aragonite and that the triangles are aligned with the b-axis and correspond to the advance of the {010} faces during the growth of the tablet. According to our interpretation, the vermiculations appear because organic molecules during growth are expelled from the a-axis, where the Ca-CO3 bonds are the shortest. In this way, the subunits forming nacre merge uninterruptedly, forming chains parallel to the a-axis, whereas the organic molecules are expelled to the sides of these chains. Hourglass patterns would be produced by preferential adsorption of organic molecules along the {010}, as compared to the {100} faces. A model is presented for the nanostructure of nacre tablets. SEM and EBSD data also show the existence within the tablets of nanocrystalline units, which are twinned on {110} with the rest of the tablet. Our study shows that the growth dynamics of nacre tablets (and bioaragonite in general) results from the interaction at two different and mutually related levels: tablets and nanogranules.

Do great spotted cuckoo nestlings beg dishonestly

It is generally assumed that begging signals provide parents with reliable information on the state of their young, allowing them to decide accordingly how much to invest in their nestlings. Avian brood-parasitic nestlings exhibit begging displays that are highly exaggerated. In most species, they also increase their begging level in relation to their level of hunger, as predicted by models of honest signalling. However, it has been suggested that great spotted cuckoo, Clamator glandarius, nestlings are an exception to this general rule because they spit out food when satiated and continue begging at a high intensity. We tested this assertion by using both natural observations of food delivery by foster parents and a laboratory experiment in which we hand-fed both cuckoo and host magpie, Pica pica, and carrion crow, Corvus corone, nestlings while controlling for the degree of food deprivation. First, we found that cuckoo nestlings did not throw out food because they are satiated. Second, as in host magpie nestlings, during a period of food deprivation the cuckoo nestlings begged at a significantly higher frequency and intensity than when fed ad libitum (a period of food abundance) and begging signals increased with an increased level of hunger in both species. These results indicate that in this cuckoo species the frequency and intensity of begging are in accordance with food requirements, and, thus, that begging is not dishonest in the sense of being unreliable.

Great spotted cuckoo fledglings are disadvantaged by magpie host parents when reared together with magpie nestlings

The post-fledging period is a critical phase for juvenile survival, and parental care provided during this period is a key component of avian reproductive performance. Very little is known about the relationships between foster parents and fledglings of brood parasites. Here, we present the results of a 5-year study about the relationships between fledglings of the non-evictor brood parasitic great spotted cuckoo (Clamator glandarius) and its magpie (Pica pica) foster parents. Sometimes, great spotted cuckoo and magpie nestlings from the same nest can fledge successfully, but most often parasitic nestlings outcompete host nestlings and only cuckoos leave the nest. We have studied several aspects of cuckoo post-fledging performance (i.e. feeding behaviour, parental defence and fledgling survival) in experimental nests in which only cuckoos or both magpie and cuckoo nestlings survived until leaving the nest. The results indicate that great spotted cuckoo fledglings reared in mixed broods together with magpie nestlings were disadvantaged by magpie adults with respect to feeding patterns. Fledgling cuckoos reared in mixed broods were fed less frequently than those reared in only cuckoo broods, and magpie adults approached less frequently to feed cuckoos from mixed broods than cuckoos from only cuckoo broods. These results imply that the presence of hosts own nestlings for comparison may be a crucial clue favouring the evolution of fledgling discrimination; and furthermore, that the risk of discrimination at the fledgling stage probably is an important selection pressure driving the evolution of the arms race between brood parasites and their hosts.

Organic membranes determine the pattern of the columnar prismatic layer of mollusc shells.

The degree to which biological control is exercised compared to physical control of the organization of biogenic materials is a central theme in biomineralization. We show that the outlines of biogenic calcite domains with organic membranes are always of simple geometries, while without they are much more complex. Moreover, the mineral prisms enclosed within the organic membranes are frequently polycrystalline. In the prismatic layer of the mollusc shell, organic membranes display a dynamics in accordance with the von Neumann–Mullins and Lewis Laws for two-dimensional foam, emulsion and grain growth. Taken together with the facts that we found instances in which the crystals do not obey such laws, and that the same organic membrane pattern can be found even without the mineral infilling, our work indicates that it is the membranes, not the mineral prisms, that control the pattern, and the mineral enclosed within the organic membranes passively adjusts to the dynamics dictated by the latter.

Great Spotted Cuckoo Fledglings Often Receive Feedings from Other Magpie Adults than Their Foster Parents: Which Magpies Accept to Feed Foreign Cuckoo Fledglings?

Natural selection penalizes individuals that provide costly parental care to non-relatives. However, feedings to brood-parasitic fledglings by individuals other than their foster parents, although anecdotic, have been commonly observed, also in the great spotted cuckoo (Clamator glandarius) – magpie (Pica pica) system, but this behaviour has never been studied in depth. In a first experiment, we here show that great spotted cuckoo fledglings that were translocated to a distant territory managed to survive. This implies that obtaining food from foreign magpies is a frequent and efficient strategy used by great spotted cuckoo fledglings. A second experiment, in which we presented a stuffed-cuckoo fledgling in magpie territories, showed that adult magpies caring for magpie fledglings responded aggressively in most of the trials and never tried to feed the stuffed cuckoo, whereas magpies that were caring for cuckoo fledglings reacted rarely with aggressive behavior and were sometimes disposed to feed the stuffed cuckoo. In a third experiment we observed feedings to post-fledgling cuckoos by marked adult magpies belonging to four different possibilities with respect to breeding status (i.e. composition of the brood: only cuckoos, only magpies, mixed, or failed breeding attempt). All non-parental feeding events to cuckoos were provided by magpies that were caring only for cuckoo fledglings. These results strongly support the conclusion that cuckoo fledglings that abandon their foster parents get fed by other adult magpies that are currently caring for other cuckoo fledglings. These findings are crucial to understand the co-evolutionary arms race between brood parasites and their hosts because they show that the presence of the hosts own nestlings for comparison is likely a key clue to favour the evolution of fledgling discrimination and provide new insights on several relevant points such as learning mechanisms and multiparasitism.

Biological strategy for the fabrication of highly ordered aragonite helices: the microstructure of the cavolinioidean gastropods.

The Cavolinioidea are planktonic gastropods which construct their shells with the so-called aragonitic helical fibrous microstructure, consisting of a highly ordered arrangement of helically coiled interlocking continuous crystalline aragonite fibres. Our study reveals that, despite the high and continuous degree of interlocking between fibres, every fibre has a differentiated organic-rich thin external band, which is never invaded by neighbouring fibres. In this way, fibres avoid extinction. These intra-fibre organic-rich bands appear on the growth surface of the shell as minuscule elevations, which have to be secreted differentially by the outer mantle cells. We propose that, as the shell thickens during mineralization, fibre secretion proceeds by a mechanism of contact recognition and displacement of the tips along circular trajectories by the cells of the outer mantle surface. Given the sizes of the tips, this mechanism has to operate at the subcellular level. Accordingly, the fabrication of the helical microstructure is under strict biological control. This mechanism of fibre-by-fibre fabrication by the mantle cells is unlike that any other shell microstructure.

Self-assembling iron oxyhydroxide/oxide tubular structures: laboratory-grown and field examples from Rio Tinto

Rio Tinto in southern Spain has become of increasing astrobiological significance, in particular for its similarity to environments on early Mars. We present evidence of tubular structures from sampled terraces in the stream bed at the source of the river, as well as ancient, now dry, terraces. This is the first reported finding of tubular structures in this particular environment. We propose that some of these structures could be formed through self-assembly via an abiotic mechanism involving templated precipitation around a fluid jet, a similar mechanism to that commonly found in so-called chemical gardens. Laboratory experiments simulating the formation of self-assembling iron oxyhydroxide tubes via chemical garden/chemobrionic processes form similar structures. Fluid-mechanical scaling analysis demonstrates that the proposed mechanism is plausible. Although the formation of tube structures is not itself a biosignature, the iron mineral oxidation gradients across the tube walls in laboratory and field examples may yield information about energy gradients and potentially habitable environments.

Transformation of ACC into aragonite and the origin of the nanogranular structure of nacre

Currently a basic tenet in biomineralization is that biominerals grow by accretion of amorphous particles, which are later transformed into the corresponding mineral phase. The globular nanostructure of most biominerals is taken as evidence of this. Nevertheless, little is known as to how the amorphous-to-crystalline transformation takes place. To gain insight into this process, we have made a high-resolution study (by means of transmission electron microscopy and other associated techniques) of immature tablets of nacre of the gastropod Phorcus turbinatus, where the proportion of amorphous calcium carbonate is high. Tablets displayed a characteristic nanoglobular structure, with the nanoglobules consisting of an aragonite core surrounded by amorphous calcium carbonate together with organic macromolecules. The changes in composition from the amorphous to the crystalline phase indicate that there was a higher content of organic molecules within the former phase. Within single tablets, the crystalline cores were largely co-oriented. According to their outlines, the internal transformation front of the tablets took on a complex digitiform shape, with the individual fingers constituting the crystalline cores of nanogranules. We propose that the final nanogranular structure observed is produced during the transformation of ACC into aragonite.

The Transport System of Nacre Components through the Surface Membrane of Gastropods

The surface membrane is a lamellar structure exclusive of gastropods that is formed during the shell secretion. It protects the surface of the growing nacre and it is located between the mantle epithelium and the mineralization compartment. At the mantle side of the surface membrane numerous vesicles provide material, and at the nacre side, the interlamellar membranes detach from the whole structure. Components of nacre (glycoproteins, polysaccharides and calcium carbonate) cross the structure to reach the mineralization compartment, but the mechanism by which this occurs is still unknown. In this paper we have investigated the ultrastructure of the surface membrane and the associated vesicle layer by means of Transmission Electron Microscopy. Electron Energy Loss Spectroscopy and Energy-dispersive X-ray Spectroscopy were used for elemental analysis. The analyses revealed the concentration of calcium in the studied structures: vesicles, surface membrane, and interlamellar membranes. We discuss the possible linkage of calcium to the organic matrix.