Ecomorphological constraints imposed by the kidney component measurements in honeyeater birds inhabiting different environments

The histological renal anatomy of 10 species of honeyeaters was examined quantitatively, using stereology. The kidneys of five species of predominantly wet zone inhabiting birds: the western spinebill Acanthorhynchus superciliosus , White-checked honeyeater Phylidonyris nigra . New Holland honeyeater Phylidonyris novaehollandiae , little wattlebird anthochaera chrysoptera and red wattlebird Anthochaera carunculata , were compared to five predominantly arid zone inhabiting birds: the grey-fronted honeyeater Meliphaga plumula , white-plumed honeyeater Meliphaga penicillata , white-fronted honeyeater Phylidonyris albifrons , spiny-checked honeyeater Acanthogenys rufogularis and yellow-throated miner Manorina flarigula. The kidneys were asymmetrical, with the left kidney being larger than the right kidney. Kidney mass was directly proportional to body mass (coefficient of correlation, r =+0·95), as was kidney volume to kidney mass (r =+1·0). Wet zone honeyeaters generally and a higher percentage and absolute volume of renal cortex, whilst arid zone honeyeaters generally had a significantly higher percentage and absolute volume of renal medulla. There were few differences between species, in either the percentage or absolute volume or luminal surface area of nephron components within the cortex. Within the medulla, wet zone honeyeaters generally had a higher percentage and absolute luminal surface area of collecting ducts, whilst arid zone honeyeaters had a higher percentage and absolute surface area of capillaries. This may be due to factors such as variations in diet and climate between habitats resulting in differences in honeyeater renal morphology which enable arid zone birds to conserve water and wet zone birds to conserve ions more efficiently.     

Measurements on the kidneys and vasa recta of various mammals in relation to urine concentrating capacity.

Maximum urine-concentrating capacity (UCC) differs widely among mammals of different species, being very high in some desert species (e.g. kangaroo rats) and very low in freshwater acquatic species (e.g. beaver). In this study, kidneys of 21 species of mammals from widely different habitats were studied in histological sections to determine whether differences in UCC can be attributed to differences in kidney structure. Parameters studied included the ratio of medullary to cortical thickness, the proportional subdivision of the medulla into inner and outer zones, and the dimensions of the vasa recta expressed in terms of the total area and the number of lumens within the vascular bundles. Determinations were made at a level where the size of individual vasa recta bundles has reached a constant maximum size, i.e. in the distal half of the outer zone. A positive correlation was found between the UCC and the ratio of medullary length to cortical thickness. No clear correlation existed between the proportion of the medullary length comprised of outer or inner zones and the UCC, although a trend to higher UCC in animals with relatively longer inner zones was apparent. Thus, it appears that the relative length of the entire medullary region is a major factor determining UCC, but the length of individual medullary zones is of lesser importance. A correlation was also found between the density of vasa recta per cubic millimeter of medullary tissue (the number of lumens regardless of identify in bundles, based on the number counted at the level sampled) and the UCC of the species. Data reported here support the view that UCC can be correlated with two parameters of kidney structure - the length of medulla relative to that of cortex and the density of vasa recta within the outer zone. It is proposed that the anatomical characteristics of the vascular supply to the medulla - that is, the vasa recta - are equally as important for the concentration of urine as is the primary mechanism determined by the characteristics of the loop of Henle and collecting ducts.     

Relative thickness of the renal medulla in birds

The intraspecific mean length of medullary cones in avian kidneys is analogous to medullary thickness in the mammalian kidney. Hence, relative medullary thickness (based upon kidney volume) can be calculated for birds as was done in mammals years ago. Comparative figures are given for 26 species from nine avian orders. The organizational pattern of cortex and medulla in the bird kidney is reviewed, and a simplified diagram of this relationship is presented. With some exceptions, urine concentrating ability and relative medullary thickness are directly proportional in mammals. Contrarily, no similar trend was evident in birds when current information on water economy was compared to relative medullary thickness in various species. There are a number of factors (such as the respective functional roles of reptilian and mammalian-type nephrons, interspecific variations in ion transport, etc.) which require study before the significance of relative thickness in the avian medulla can be evaluated more thoroughly.     

Relationships between renal morphology and diet in 26 species of new world bats (suborder microchiroptera)

The renal morphology of 24 species of mormoopid and phyllostomid bats feeding on six different diets was examined to test evolutionary changes in several structural traits presumably led by dietary shifts from ancestral insectivorous diets. The kidneys of a fish-eating vespertilionid and an insect-eating emballonurid were also examined but not included in the phylogenetic comparison. The length, width, and breadth of the kidneys were used to calculate relative medullary thickness (RMT). Tissues were processed for stereological analysis, and the volumes of the kidney, nephron components, and vasculature were determined. RMT did not correlate with body mass in either animal-eating or plant-eating phyllostomid and mormoopid bats. The shift from insectivory to frugivory and nectarivory was accompanied by a reduction in RMT, a reduction in the percent of renal medulla, and an increase in the percent of renal cortex. No changes in these traits were observed in bats that shifted to carnivorous, omnivorous or sanguinivorous habits. No changes were observed in renal vasculature, in the percentage of cortical and medullary nephron components or of capillaries surrounding the nephrons in any feeding group. Vespertilionid and emballonurid species had similar values in all traits examined as compared to insectivorous phyllostomids and mormoopids. Our data suggest that diet does not influence a single area of the nephron, but rather the entire nephron such that the relative amounts of renal cortex and medulla are affected.     

Functional morphology of the avian medullary cone

The organization of the renal medulla of the Gambel's quail, Callipepla gambelii, kidney was examined to determine the number of loops of Henle and collecting ducts and the surface area occupied by the different nephron segments as a function of distance down the medullary cones. Eleven medullary cones were dissected from the kidneys of four birds, and the tissue was processed and sectioned for light microscopy. In addition, individual nephrons were isolated on which total loop thin descending segment and thick prebend segment lengths were measured. The results show no correlation between the absolute number of loops of Henle and the length of the medullary cones. The number of thick and thin limbs of Henle and collecting ducts decrease exponentially with distance toward the apex of the cones and the rate of decrease is similar for cones of different lengths. Initially there is a rapid decrease in the number of thin limbs of Henle, indicating that most nephrons do not penetrate the cones a great distance. Thick descending limbs of Henle (prebend segment) ranged in length from 50 to 770 microm, and there was little correlation with the total length of the loop of Henle. However, the length of the thin limb of Henle correlated well with total loop length. The cell surface areas of the limbs of the loop of Henle and the collecting ducts decreased toward the apex of the cones.     

The isotopic composition and insect content of diet predict tissue isotopic values in a South American passerine assemblage

We analyzed the carbon and nitrogen isotopic values of the muscle, liver, and crop contents (“diet”) of 132 individuals of 16 species of Chilean birds. The nitrogen content of diet was tightly correlated with the fraction of gut contents represented by insects relative to plant material. The carbon and nitrogen isotopic values of diet, liver, and muscle were all linearly correlated, implying high temporal consistency in the isotopic value of the diet of these birds. However, δ¹⁵N was not significantly related with the percentage of insects in diet. These results cast doubt on the applicability of the use of ¹⁵N enrichment to diagnose trophic level in, at least some, terrestrial ecosystems. However, the residuals of the relationship relating the isotopic value of bird tissues with those of their diet were weakly negatively correlated with insect intake. We hypothesize that this negative correlation stems from the higher quality of protein found in insects relative to that of plant materials. Finally, our data corroborated a perplexing and controversial negative relationship between tissue to diet isotopic discrimination and the isotopic value of diet. We suggest that this relationship is an example of the commonly observed regression to the mean effect that plagues many scientific studies.     

The diet of feral cats on islands: a review and a call for more studies

Cats are among the most successful and damaging invaders on islands and a significant driver of extinction and endangerment. Better understanding of their ecology can improve effective management actions such as eradication. We reviewed 72 studies of insular feral cat diet from 40 islands worldwide. Cats fed on a wide range of species from large birds and medium sized mammals to small insects with at least 248 species consumed (27 mammals, 113 birds, 34 reptiles, 3 amphibians, 2 fish and 69 invertebrates). Three mammals, 29 birds and 3 reptiles recorded in the diet of cats are listed as threatened by the IUCN. However, a few species of introduced mammals were the most frequent prey, and on almost all islands mammals and birds contributed most of the daily food intake. Latitude was positively correlated with the predation of rabbits and negatively with the predation of reptiles and invertebrates. Distance from landmass was positively correlated with predation on birds and negatively correlated with the predation of reptiles. The broad range of taxa consumed by feral cats on islands suggests that they have the potential to impact almost any native species, even the smallest ones under several grams, that lack behavioral, morphological or life history adaptations to mammalian predators. Insular feral cat??s reliance on introduced mammals, which evolved with cat predation, suggests that on many islands, populations of native species have already been reduced.     

Water restriction increases renal inner medullary manganese superoxide dismutase (MnSOD)

Oxidative stress damages cells. NaCl and urea are high in renal medullary interstitial fluid, which is necessary to concentrate urine, but which causes oxidative stress by elevating reactive oxygen species (ROS). Here, we measured the antioxidant enzyme superoxide dismutases (SODs, MnSOD, and Cu/ZnSOD) and catalase in mouse kidney that might mitigate the oxidative stress. MnSOD protein increases progressively from the cortex to the inner medulla, following the gradient of increasing NaCl and urea. MnSOD activity increases proportionately, but MnSOD mRNA does not. Water restriction, which elevates renal medullary NaCl and urea, increases MnSOD protein, accompanied by a proportionate increase in MnSOD enzymatic activity in the inner medulla, but not in the cortex or the outer medulla. In contrast, Cu/ZnSOD and TNF-α (an important regulator of MnSOD) do not vary between the regions of the kidney, and expression of catalase protein actually decreases from the cortex to the inner medulla. Water restriction increases activity of mitochondrial enzymes that catalyze production of ROS in the inner medulla, but reduces NADPH oxidase activity there. We also examined the effect of high NaCl and urea on MnSOD in Madin-Darby canine kidney (MDCK) cells. High NaCl and high urea both increase MnSOD in MDCK cells. This increase in MnSOD protein apparently depends on the elevation of ROS since it is eliminated by the antioxidant N-acetylcysteine, and it occurs without raising osmolality when ROS are elevated by antimycin A or xanthine oxidase plus xanthine. We conclude that ROS, induced by high NaCl and urea, increase MnSOD activity in the renal inner medulla, which moderates oxidative stress.     

Loss of renal medullary endothelin B receptor function during salt deprivation is regulated by angiotensin II

We have recently demonstrated that chronic infusion of exogenous ANG II, which induces blood pressure elevation, attenuates renal medullary endothelin B (ET(B)) receptor function in rats. Moreover, this was associated with a reduction of ET(B) receptor expression in the renal inner medulla. The aim of this present work was to investigate the effect of a physiological increase in endogenous ANG II (low-salt diet) on the renal ET system, including ET(B) receptor function. We hypothesized that endogenous ANG II reduces renal medullary ET(B) receptor function during low-salt intake. Rats were placed on a low-salt diet (0.01-0.02% NaCl) for 2 wk to allow an increase in endogenous ANG II. In rats on normal-salt chow, the stimulation of renal medullary ET(B) receptor by ET(B) receptor agonist sarafotoxin 6c (S6c) causes an increase in water (3.6 ± 0.4 from baseline vs. 10.5 ± 1.3 μl/min following S6c infusion; P < 0.05) and sodium excretion (0.38 ± 0.06 vs. 1.23 ± 0.17 μmol/min; P < 0.05). The low-salt diet reduced the ET(B)-dependent diuresis (4.5 ± 0.5 vs. 6.1 ± 0.9 μl/min) and natriuresis (0.40 ± 0.11 vs. 0.46 ± 0.12 μmol/min) in response to acute intramedullary infusion of S6c. Chronic treatment with candesartan restored renal medullary ET(B) receptor function; urine flow was 7.1 ± 0.9 vs. 15.9 ± 1.7 μl/min (P < 0.05), and sodium excretion was 0.4 ± 0.1 vs. 1.1 ± 0.1 μmol/min (P < 0.05) before and after intramedullary S6c infusion, respectively. Receptor binding assays determined that the sodium-depleted diet resulted in a similar level of ET(B) receptor binding in renal inner medulla compared with rats on a normal-salt diet. Candesartan reduced renal inner medullary ET(B) receptor binding (1,414 ± 95 vs. 862 ± 50 fmol/mg; P < 0.05). We conclude that endogenous ANG II attenuates renal medullary ET(B) receptor function to conserve sodium during salt deprivation independently of receptor expression.     

Developmental immunolocalization of heat shock protein 70 (HSP70) in epithelial cell of rat kidney

During renal development the cells in the medulla are exposed to elevated and variable interstitial osmolality. Heat shock protein 70 (HSP70) is a major molecular chaperone and plays an important role in the protection of cells in the renal medulla from high osmolality. The purpose of this study was to establish the time of immunolocalization and distribution of HSP70 in developing and adult rat kidney. In addition, changes in HSP70 immunolocalization following the infusion of furosemide were investigated. In adult animals, the HSP70 was expressed in the medullary thin ascending limb of Henle's loop (ATL) and inner medullary collecting duct (IMCD). In developing kidney, HSP70 immunoreactivity was first detected in the IMCD of the papillary tip on postnatal day 1. From four to 14 days of age, HSP70 was detected in the ATL after transformation from thick ascending limb, beginning at the papillary tip and ascending to the border between the outer and inner medulla. The immunolocalization of HSP70 in both the ATL and IMCD gradually increased during two weeks. The gradual increase in HSP70 was associated with an increase in its mRNA abundance. However, furosemide infusion resulted in significantly reduced HSP70 immunolocalization in the IMCD and ATL. These data demonstrated that the expression of HSP70 was closely correlated with changes in interstitial osmolality during the development of the kidney. We suggest that HSP70 protects ATL and IMCD cells in the inner medulla from the stress of high osmolality and may be involved in the transformation of the ATL of the long loop of Henle during renal development.     

Diet and habitat aridity affect osmoregulatory physiology: An intraspecific field study along environmental gradients in the Rufous-collared sparrow

The urine field osmolality in Zonotrichia capensis along a latitudinal gradient in rainfall and temperature in Chile was examined. We also investigated latitudinal variation in the renal traits that mediate how these birds cope with dehydration. We used the δ¹⁵N of this species' tissue to investigate whether the reliance on animals and seeds varied among birds and if it had any effect on excretion and renal traits. We found a significant latitudinal variation in urine osmolality, a variable that was correlated with habitat aridity. We also found that the kidney size and proportion of kidney devoted to medullary tissue differed between birds from arid and mesic localities, but not in a lineal fashion with aridity. The increment in the position in the food web, as measured by δ¹⁵N, led to an increment in urine osmolality, without changes in kidney features. Our data suggested that differences in dietary habits in the field could be not extended enough to cause changes in the kidney structure in Rufous-collared sparrows.     

Overexpression of HIF Prolyl‐Hydoxylase‐2 transgene in the renal medulla induced a salt sensitive hypertension

Renal medullary hypoxia‐inducible factor (HIF)‐1α and its target genes, such as haem oxygenase and nitric oxide synthase, have been indicated to play an important role in the regulation of sodium excretion and blood pressure. HIF prolyl hydroxylase domain‐containing proteins (PHDs) are major enzymes to promote the degradation of HIF‐1α. We recently reported that high salt intake suppressed the renal medullary PHD2 expression and thereby activated HIF‐1α‐mediated gene regulation in the renal medulla in response to high salt. To further define the functional role of renal medullary PHD2 in the regulation of renal adaptation to high salt intake and the longer term control of blood pressure, we transfected PHD2 expression plasmids into the renal medulla in uninephrectomized rats and determined its effects on pressure natriuresis, sodium excretion after salt overloading and the long‐term control of arterial pressure after high salt challenge. It was shown that overexpression of PHD2 transgene increased PHD2 levels and decreased HIF‐1α levels in the renal medulla, which blunted pressure natriuresis, attenuated sodium excretion, promoted sodium retention and produced salt sensitive hypertension after high salt challenge compared with rats treated with control plasmids. There was no blood pressure change in PHD2‐treated rats that were maintained in low salt diet. These results suggested that renal medullary PHD2 is an important regulator in renal adaptation to high salt intake and a deficiency in PHD2‐mediated molecular adaptation in response to high salt intake in the renal medulla may represent a pathogenic mechanism producing salt sensitive hypertension.     

Effect of vanadate administration on polyol pathway in diabetic rat kidney.

Effect of oral administration of sodium orthovanadate for three weeks on polyol pathway in renal cortex and medulla was studied in control and alloxan diabetic rats. An enhancement in aldose reductase in cortex and medulla and sorbitol dehydrogenase in cortex was observed in alloxan diabetic rats. Despite depressed insulin secretion, vanadate treatment to diabetic rats counteracted hyperglycemia, normalized elevated enzyme activities and glucose level, prevented medullary sorbitol accumulation and markedly checked increase in kidney weight. These results show that vanadate causes marked improvement in renal hypertrophy and has an antidiabetogenic effect on polyol pathway in diabetic kidney.     

Development of the kidney medulla

The mature renal medulla, the inner part of the kidney, consists of the medullary collecting ducts, loops of Henle, vasa recta and the interstitium. The unique spatial arrangement of these components is essential for the regulation of urine concentration and other specialized kidney functions. Thus, the proper and timely assembly of medulla constituents is a crucial morphogenetic event leading to the formation of a functioning metanephric kidney. Mechanisms that direct renal medulla formation are poorly understood. This review describes the current understanding of the key molecular and cellular mechanisms underlying morphological aspects of medulla formation. Given that hypoplasia of the renal medulla is a common manifestation of congenital obstructive nephropathy and other types of congenital anomalies of the kidney and urinary tract (CAKUT), better understanding of how disruptions in medulla formation are linked to CAKUT will enable improved diagnosis, treatment and prevention of CAKUT and their associated morbidity.     

Phenotypic variation of an alien species in a new environment: the body size and diet of American mink over time and at local and continental scales

Introduced species must adapt their ecology, behaviour, and morphological traits to new conditions. The successful introduction and invasive potential of a species are related to its levels of phenotypic plasticity and genetic polymorphism. We analysed changes in the body mass and length of American mink (Neovison vison) since its introduction into the Warta Mouth National Park, western Poland, in relation to diet composition and colonization progress from 1996 to 2004. Mink body mass decreased significantly during the period of population establishment within the study area, with an average decrease of 13% from 1.36 to 1.18 kg in males and of 16% from 0.83 to 0.70 kg in females. Diet composition varied seasonally and between consecutive years. The main prey items were mammals and fish in the cold season and birds and fish in the warm season. During the study period the proportion of mammals preyed upon increased in the cold season and decreased in the warm season. The proportion of birds preyed upon decreased over the study period, whereas the proportion of fish increased. Following introduction, the strictly aquatic portion of mink diet (fish and frogs) increased over time, whereas the proportion of large prey (large birds, muskrats, and water voles) decreased. The average yearly proportion of large prey and average‐sized prey in the mink diet was significantly correlated with the mean body masses of males and females. Biogeographical variation in the body mass and length of mink was best explained by the percentage of large prey in the mink diet in both sexes, and by latitude for females. Together these results demonstrate that American mink rapidly changed their body mass in relation to local conditions. This phenotypic variability may be underpinned by phenotypic plasticity and/or by adaptation of quantitative genetic variation. The potential to rapidly change phenotypic variation in this manner is an important factor determining the negative ecological impacts of invasive species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 681–693.     

Development of the kidney medulla

The mature renal medulla, the inner part of the kidney, consists of the medullary collecting ducts, loops of Henle, vasa recta and the interstitium. The unique spatial arrangement of these components is essential for the regulation of urine concentration and other specialized kidney functions. Thus, the proper and timely assembly of medulla constituents is a crucial morphogenetic event leading to the formation of a functioning metanephric kidney. Mechanisms that direct renal medulla formation are poorly understood. This review describes the current understanding of the key molecular and cellular mechanisms underlying morphological aspects of medulla formation. Given that hypoplasia of the renal medulla is a common manifestation of congenital obstructive nephropathy and other types of congenital anomalies of the kidney and urinary tract (CAKUT), better understanding of how disruptions in medulla formation are linked to CAKUT will enable improved diagnosis, treatment and prevention of CAKUT and their associated morbidity.     

Endogenous Carbamylation of Renal Medullary Proteins

Protein carbamylation is a post-translational modification that can occur in the presence of urea. In solution, urea is in equilibrium with ammonium cyanate, and carbamylation occurs when cyanate ions react with the amino groups of lysines, arginines, protein N-termini, as well as sulfhydryl groups of cysteines. The concentration of urea is elevated in the renal inner medulla compared with other tissues. Due to the high urea concentration, we hypothesized that carbamylation can occur endogenously within the rat inner medulla. Using immunoblotting of rat kidney cortical and medullary homogenates with a carbamyl-lysine specific antibody, we showed that carbamylation is present in a large number of inner medullary proteins. Using protein mass spectrometry (LC-MS/MS) of rat renal inner medulla, we identified 456 unique carbamylated sites in 403 proteins, including many that play important physiological roles in the renal medulla [Data can be accessed at https://helixweb.nih.gov/ESBL/Database/Carbamylation/Carbamylation_peptide_sorted.html]. We conclude that protein carbamylation occurs endogenously in the kidney, modifying many physiologically important proteins.     

Salicylate nephropathy in the Gunn rat: potential role of prostaglandins

We examined the potential role of prostaglandins in the development of analgesic nephropathy in the Gunn strain of rat. The homozygous Gunn rats have unconjugated hyperbilirubinemia due to the absence of glucuronyl transferase, leading to marked bilirubin deposition in renal medulla and papilla. These rats are also highly susceptible to develop papillary necrosis with analgesic administration. We used homozygous (jj) and phenotypically normal heterozygous (jJ) animals. Four groups of rats (n = 7) were studied: jj and jJ rats treated either with aspirin 300 mg/kg every other day or sham-treated. After one week, slices of cortex, outer and inner medulla from one kidney were incubated in buffer and prostaglandin synthesis was determined by radioimmunoassay. The other kidney was examined histologically. A marked corticomedullary gradient of prostaglandin synthesis was observed in all groups. PGE2 synthesis was significantly higher in outer medulla, but not cortex or inner medulla, of jj (38 +/- 6 ng/mg prot) than jJ rats (15 +/- 3) (p less than 0.01). Aspirin treatment reduced PGE2 synthesis in all regions, but outer medullary PGE2 remained higher in jj (18 +/- 3) than jJ rats (9 +/- 2) (p less than 0.05). PGF2 alpha was also significantly higher in the outer medulla of jj rats with and without aspirin administration (p less than 0.05). The changes in renal prostaglandin synthesis were accompanied by evidence of renal damage in aspirin-treated jj but not jJ rats as evidenced by: increased incidence and severity of hematuria (p less than 0.01); increased serum creatinine (p less than 0.05); and increase in outer medullary histopathologic lesions (p less than 0.005 compared to either sham-treated jj or aspirin-treated jJ). These results suggest that enhanced prostaglandin synthesis contributes to maintenance of renal function and morphological integrity, and that inhibition of prostaglandin synthesis may lead to pathological renal medullary lesions and deterioration of renal function.     

Evidence that dopaminergic sympathetic axons supply the medullary arterioles of human kidney

Summary The ability of the kidney to excrete sodium appears to depend on release of dopamine from intrarenal sources. In the present study, we have used immunohistochemistry to examine the possibility that renal dopaminergic nerves constitute one of these sources. We found that the sympathetic axons supplying cortical structures in human kidney contain tyrosine hydroxylase-like immunoreactivity but lack DOPA decarboxylase-like immunoreactivity. By contrast, the vasa recta arterioles of the renal medulla are supplied by varicose tyrosine hydroxylase-positive nerve fibres, some of which also contain DOPA decarboxylase. As DOPA decarboxylase has been demonstrated in other situations to be a selective marker for dopaminergic terminal axons, our results suggest the innervation of renal medullary blood vessels in man by both noradrenergic and dopaminergic sympathetic nerves.