Zeev Arad

The effect of bat (Rousettus aegyptiacus) dispersal on seed germination in eastern Mediterranean habitats

The fruit-bat Rousettus aegyptiacus (Pteropodidae) in Israel consumes a variety of cultivated and wild fruits. The aim of this study was to explore some of its qualities as a dispersal agent for six fruit-bearing plant species. The feeding roosts of the fruit-bat are located an average of 30 m from its feeding trees and thus the bats disperse the seeds away from the shade of the parent canopy. The bat spits out large seeds but may pass some (2%) of the small seeds (<4 mg) through its digestive tract. However, neither the deposited seeds nor the ejected seeds (except in one case) had a significantly higher percentage germinating than intact seeds. Although the fruit-bat did not increase the percentage germinating, seeds of three plant species subject to different feeding behaviors (deposited in feces or spat out as ejecta) had a different temporal pattern of germination from the intact seeds. The combined seed germination distribution generated by these different treatments is more even over time than for each treatment alone. It is sugested that this increases asynchronous germination and therefore enhances plant fitness by spreading the risks encountered during germination, especially in eastern Mediterranean habitats where the pattern of rainfall is unpredictable.

Is the Egyptian fruit-bat Rousettus aegyptiacus a pest in Israel? An analysis of the bat's diet and implications for its conservation

The Egyptian fruit-bat Rousettus aegyptiacus is regarded as a pest for agriculture. However, no quantitative data on its diet have been collected in Israel or in other Mediterranean areas, and control measures in the past reduced populations of insectivorous bats in Israel. We therefore studied the relative importance of native versus commercially cultivated fruit plants by analysis of bat faeces. Droppings were collected during 1993‐1995 in two roost-sites in the Carmel National Park. Results show that the bat feeds mainly on fruits but leaves and pollen are also eaten. Leaf eating was observed mainly during winter, when bats may face times of severe decrease in fruit availability and quality. Only four fruit species (15%) of the bat’s diet are commercially grown and only two of these in the research area. Therefore the definition of the fruit-bat as a major agricultural pest should be re-examined. Two eAective methods for controlling damage caused by bats are discussed. # 1999 Published by Elsevier Science Ltd. All rights reserved.

Nitrogen and Energy Balance of the Fruit Bat Rousettus aegyptlacus on Natural Fruit Diets

The nitrogen and energy balances of the Egyptian fruit bat, Rousettus aegyptiacus (Pteropodidae), were determined in a series of studies of animals on five single-fruit diets differing in their nutritional content (carob, Ceratonoia siliqua; Persian lilac, Melia azedarach; loquat, Eriobotrya japponica; mulberry, Murus nigra; and sycamore, Ficus sycomorus). It was found that except for Persian lilac, these fruits, which are eaten in nature by the bats, can adequately supply their nitrogen requirements, while Persian lilac and loquat were insufficient for their energy demands. On the basis of average nutrient composition across the tested fruits, the Egyptian fruit bat (mean body mass 144 g) requires a mean intake of 6g dry matter per day for maintaining nitrogen balance, while a mean intake of 11 g dry matter per day is needed in order to fulfill its daily energy requirements. These results suggest that energy, rather than nitrogen, is the limiting nutritional component in the diet of the fruit bat. The maintenance nitrogen requirement determined from the balance studies, 0.247 g N kg-0.75 d⁻¹, is 55% lower than expected from allometric relations. When the lilac diet is excluded, it is even lower: 0.110 g N kg-0.75 d⁻¹ (76% lower than expected). The maintenance nitrogen requirement is also much lower than reported for other species of fruit bats. This may reflect an adaptation to periods of low fruit availability and thus nitrogen shortage within the distribution limits of R. aegyptiacus.

Heat shock proteins and resistance to desiccation in congeneric land snails

Land snails are subject to daily and seasonal variations in temperature and in water availability and depend on a range of behavioral and physiological adaptations for coping with problems of maintaining water, ionic, and thermal balance. Heat shock proteins (HSPs) are a multigene family of proteins whose expression is induced by a variety of stress agents. We used experimental desiccation to test whether adaptation to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desiccation-resistant, desert species Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species Sphincterochila cariosa. We examined the HSP response in the foot, hepatopancreas, and kidney tissues of snails exposed to normothermic desiccation. Our findings show variations in the HSP response in both timing and magnitude between the two species. The levels of endogenous Hsp72 in S. cariosa were higher in all the examined tissues, and the induction of Hsp72, Hsp74, and Hsp90 developed earlier than in S. zonata. In contrary, the induction of sHSPs (Hsp25 and Hsp30) was more pronounced in S. zonata compared to S. cariosa. Our results suggest that land snails use HSPs as part of their survival strategy during desiccation and as important components of the aestivation mechanism in the transition from activity to dormancy. Our study underscores the distinct strategy of HSP expression in response to desiccation, namely the delayed induction of Hsp70 and Hsp90 together with enhanced induction of sHSPs in the desert-dwelling species, and suggests that evolution in harsh environments will result in selection for reduced Hsp70 expression.

How do cormorants counter buoyancy during submerged swimming

SUMMARY Buoyancy is a de-stabilizing force for diving cormorants that forage at shallow depths. Having to counter this force increases the cost of transport underwater. Cormorants are known to be less buoyant than most water birds but are still highly buoyant (ρ=∼0.8 kg m–3) due to their adaptations for aerial flight. Nevertheless, cormorants are known to dive at a wide range of depths, including shallow dives where buoyancy is maximal. We analyzed the kinematics of underwater swimming of the great cormorant (Phalacrocorax carbo sinensis) in a shallow pool to discover and evaluate the mechanisms countering buoyancy while swimming horizontally. The birds maintained a very uniform cyclic paddling pattern. Throughout this cycle, synchronized tilting of the body, controlled by the tail, resulted in only slight vertical drifts of the center of mass around the average swimming path. We suggest that this tilting behavior serves two purposes: (1) the elongated bodies and the long tails of cormorants, tilted at a negative angle of attack relative to the swimming direction, generate downward directed hydrodynamic lift to resist buoyancy and (2) during the propulsive phase, the motion of the feet has a significant vertical component, generating a vertical component of thrust downward, which further helps to offset buoyancy. The added cost of the drag resulting from this tilting behavior may be reduced by the fact that the birds use a burst-and-glide pattern while swimming.

Cormorants keep their power: visual resolution in a pursuit-diving bird under amphibious and turbid conditions.

Cormorants (Aves; Phalacrocoracidae) are active fliers, yet they forage by pursuit diving and capture of fish with the bill. In air, the cormorant’s cornea provides most of the total refractive power of the eye [1]. Underwater, however, corneal power is lost, as the cornea is now bathed in liquids of similar refractive index. The retention of a sharp image, while performing precise visual tasks underwater, requires that the cormorant’s optical system compensates for the loss of refractive power of the cornea. In addition, the underwater photic environment differs markedly from the aerial one, with the image quality undergoing a rapid deterioration through scatter and absorption [2,3]. Upon submergence, cormorants compensate for the loss of corneal power (>55 dioptres, D) and rapidly (>1000 D/sec) attain a state of emmetropia, i.e. they are well focussed [4], by marked changes in the shape of their very flexible lens [1,5]. However, the visual capacities of pursuit-diving birds under the optical demands imposed by moving from one medium to another and the respective differences in the photic environments have not been determined to date. We tested the aerial and underwater visual resolution of the great cormorant (Phalacrocorax carbo sinensis) for high contrast, square wave gratings. Stimuli were presented in a forced choice situation (ymaze) under high levels of natural illumination. Visual resolution was calculated from gratings of given bar widths at given distances from the y-junction to the stimuli. In clear water, the cormorants’ resolution was 8.9′ ± 0.5′ (minutes of arc, mean ± s.e, n = 5, range 10.4′ – 7.8′; Figure 1A), while in air it was 3.8′ ± 0.3′ (n = 3, range 4.3′ – 3.3′; Figure 1B). The birds’ choice underwater was performed while they swam at ~1.7 m/sec so that the testing of resolution replicated the naturally occurring dynamic discrimination of underwater events. The position at which an actual choice was made could be determined from the abrupt change in the orientation of the head toward the stimulus. In all tests, the choice was made between ~60 and 90 cm before the y-junction. Calculating underwater visual resolution for the positions of choice provided a value of 6.3′ ± 0.4′ (n = 5) underwater and 3.1′ ± 0.3′ (n = 3) in air. While vision is regarded as the major modality used in the detection and capture of prey by pursuit-diving birds, this is the first quantitative estimate of the amphibious visual capacity in any bird. Compared with other bird species, the cormorants’ resolution in air (Supplemental Table 1) was relatively low in both absolute terms (Figure 1C) and when body mass [6,7] or eye height above the ground [8] were considered. The cormorants’ resolution underwater was comparable with the higher values reported for fishes [9], Pinnipeds (e.g., seals, sea lions) [10] and Cetaceans (e.g., killer whales, dolphins) [11] (Figure 1C). Because visual resolution in single chambered eyes tends to increase with eye size [6,7], it was expected that cormorants, with corneo-scleral diameters of ~18–19 mm will have a lower resolution than aquatic mammals having eye diameters of ~20 mm (dolphins) and ~50 mm (baleen whales). The requirements to perform precise visuo-motor tasks in two optically different media, and the uniqueness of the lenticular system of these birds [1,5] make the vision of pursuitdiving birds a model of vertebrate capacities at the extreme. Performing visual tasks underwater is hindered by the rapid degradation of image brightness and contrast due to scatter and absorption of light by water molecules and by suspended particles (turbidity) [2]. We tested the visual resolution of cormorants (n = 5) under controlled, low levels of water turbidity (< 3 nephlometric turbidity units; NTU). The minimal resolvable stripe width was linearly correlated with turbidity (y = 3.71x + 7.6; R2 = 0.98; p < 0.001), hence, resolution declined with increasing turbidity within the tested range. The results obtained for clear water (~0.2 NTU) fitted the regression line well. Experimental results on the effects of turbidity on visually guided behavior of aquatic vertebrates are uncommon and, in fishes, are confined mostly to turbidity levels higher than 3 NTU and to the use of reactive distance as a behavioral measure [12]. Our results show that turbidity levels lower than 1 NTU have a clear effect on image formation underwater and consequently on the underwater visual environment in general. Low turbidity levels are commonly encountered in natural water bodies and thus are of crucial importance in our understanding of the evolution, sensory ecology, and microhabitat selection in aquatic organisms [13–15].

Natural annual cycle of heat shock protein expression in land snails: desert versus Mediterranean species of Sphincterochila.

SUMMARY Land snails are subject to daily and seasonal variations in temperature and in water availability, and have evolved annual cycles of activity and aestivation as part of their survival strategy. We tested in the field whether adaptation to different habitats affects the endogenous levels of heat shock proteins (HSPs) in two closely related Sphincterochila snail species, a desiccation-resistant desert species, Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species, S. cariosa. We examined HSP levels in various tissues of snails during aestivation and after resumption of activity. Our study shows that, during aestivation, S. cariosa had higher standing stocks of Hsp70 in the foot and the hepatopancreas, and of small HSPs (sHSPs) in all the examined tissues, whereas S. zonata had higher stocks of Hsp70 in the kidney and of Hsp90 in the kidney and in the hepatopancreas. Arousal induced a general upregulation of HSPs, except for Hsp90, the expression of which in the foot was higher during aestivation. We suggest that the stress protein machinery is upregulated during arousal in anticipation of possible oxidative stress ensuing from the accelerating metabolic rate and the exit from the deep hypometabolic state. Our findings support the concept that, in land snails, aestivation and activity represent two distinct physiological states, and suggest that land snails use HSPs as important components of the aestivation mechanism, and as part of their survival strategy during and after arousal. Our study also indicates that adaptation to different habitats results in the development of distinct strategies of HSP expression with likely consequences for the ecology and distribution of land snails.

Dietary protein influences the rate of 15N incorporation in blood cells and plasma of Yellow-vented bulbuls (Pycnonotus xanthopygos).

SUMMARY The rate at which an animals tissues incorporate the isotopic composition of food determines the time window during which ecologists can discern diet changes. We investigated the effect of protein content in the diet on the incorporation rate of 15N into the plasma proteins and blood cells of Yellow-vented bulbuls (Pycnonotus xanthopygos). Using model comparison analyses, we found that one-compartment models described incorporation data better than two-compartment models. Dietary protein content had a significant effect on the residence time of 15N in plasma proteins and blood cells. The diet with the highest protein content led to a 15N retention time of 21 and 5 days for cells and plasma, respectively. In contrast, average 15N retention time in the cells and plasma of birds fed on the diet with the lowest protein was 31 and 7 days, respectively. The isotopic discrimination factorΔ 15N=δ15Ntissues–δ15Ndiet was also dependent on dietary protein content, and was lowest in birds fed the diet with the highest protein content. Blood, plasma and excreta were enriched in 15N relative to diet. In contrast, ureteral urine was either significantly depleted of 15N in birds fed the diet with the lowest protein content or did not differ in δ15N from the diets with the intermediate and high protein content. Thus, isotopic incorporation rates and tissue-to-diet discrimination factors cannot be considered fixed, as they depend on diet composition.

DIETARY IMPLICATIONS OF INTRAPOPULATION VARIATION IN NITROGEN ISOTOPE COMPOSITION OF AN OLD WORLD FRUIT BAT

Abstract We used nitrogen isotope analysis from pectoral muscle of the Egyptian fruit bat Rousettus aegyptiacus (Chiroptera: Pteropodidae) to determine intrapopulation variation in sources of dietary protein throughout the year in northern Israel. In Mediterranean climates, winter and summer are stable seasons, whereas spring and fall are transitional seasons. Number of species of fruit-bearing plants is higher during the transitional periods, and we therefore predicted that intrapopulation variation would be higher during spring than in winter and summer; we made no prediction for fall because sample size was small. We also reconstructed sources of dietary protein for each individual using nitrogen isotope ratios (δ15N) to determine whether individuals foraged on the same sources of food within each season. Intrapopulation variation in δ15N was significantly higher in spring (δ15N range: 9.7–17.5‰) compared to winter (8.8–11.1‰) and summer (9.5–11.2‰), suggesting that individuals during this period varied more in their use of protein sources. Dietary reconstruction revealed intrapopulation partitioning among the bats in the use of plant food items, and interspecific partitioning among plants in their dependence on dispersal by bats.

Metabolism and thermoregulation in the Levant vole Microtus guentheri: the role of photoperiodicity

Abstract 1. 1. The populations of the Levant vole, Microtus guentheri, inhabiting the Mediterranean ecosystem of Israel, are marginal populations which seem to be well adapted to its long dry and warm season. The thermoregulatory and metabolic responses of the Levant voles of Israel to manipulation of photoperiod were studied to assess to role of photoperiodicity in seasonal acclimatization. 2. 2. Resting metabolic rate (RMR) and body temperature at various ambient temperatures, overall thermal conductance, nonshivering thermogenesis, gross energy and digestible energy intake were measured in voles acclimated to long scotophase (8L:16D) and long photophase (16L:8D) at a constant ambient temperature of 25±1°C. 3. 3. This study revealed that acclimation to a long photophase resulted in a decreased RMR and minimal thermal conductance, but in a higher upper critical point of the thermoneutral zone, as well as higher gross energy and digestible energy intakes and in a higher body mass. 4. 4. Therefore, we suggest that an increased photophase is an important environmental cue for summer acclimatization of the metabolic and thermoregulatory systems in the Levant vole.