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Nonbreeding Eastern Curlews Numenius Madagascariensis Do Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology Nonbreeding Eastern Curlews Numenius madagascariensis Do Not Increase the Rate of Intake or Digestive Efficiency before Long‐Distance Migration because of an Apparent Digestive Constraint Author(s): Yuri Zharikov and Gregory A. Skilleter Source: Physiological and Biochemical Zoology, Vol. 76, No. 5 (September/October 2003), pp. 704-715 Published by: The University of Chicago Press. Sponsored by the Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology Stable URL: http://www.jstor.org/stable/10.1086/376427 . Accessed: 04/11/2015 23:25 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press and Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology are collaborating with JSTOR to digitize, preserve and extend access to Physiological and Biochemical Zoology. http://www.jstor.org This content downloaded from 23.235.32.0 on Wed, 4 Nov 2015 23:25:52 PM All use subject to JSTOR Terms and Conditions 704 Nonbreeding Eastern Curlews Numenius madagascariensis Do Not Increase the Rate of Intake or Digestive Efficiency before Long- Distance Migration because of an Apparent Digestive Constraint Yuri Zharikov1,* Introduction Gregory A. Skilleter2 Long-distance migratory birds deposit large amounts of excess 1Department of Biological Sciences, Simon Fraser University, tissue, both lipids and proteins, to allow for successful migra- Burnaby, British Columbia V5A 1S6, Canada; 2Marine and tion between the nonbreeding (wintering) and breeding Estuarine Ecology Unit, Department of Zoology and grounds (Alerstam and Lindstro¨m 1990; Lindstro¨m and Entomology, University of Queensland, Brisbane QLD 4072, Piersma 1993). This requires a considerable increase in daily Australia energy consumption before migration. Such an increase can be achieved by prolonging periods of foraging and/or increasing Accepted 4/1/03 the rate of energy intake (Blem 1980; Zwarts et al. 1990a, 1990b). There are two ways for a bird to increase the rate of energy intake. One is to improve the efficiency of digestion of ABSTRACT consumed food, thus increasing the rate of energy intake with- out increasing the rate of food consumption (Scott et al. 1994; The possibility of premigratory modulation in gastric digestive Bairlein 2002). So far, there is little empirical evidence to suggest performance was investigated in a long-distance migrant, the that this strategy is widespread in nature (Karasov 1996). How- eastern curlew (Numenius madagascariensis), in eastern Aus- ever, this may be due to the lack of studies addressing the issue tralia. The rate of intake in the curlews was limited by the rate (e.g., Hume and Biebach 1996). The other way, which is very of digestion but not by food availability. It was hypothesized common among birds, is to increase the rate of food con- that before migration, eastern curlews would meet the increased sumption per se (e.g., Blem 1980; Karasov 1996; Karasov and energy demand by increasing energy consumption. It was pre- Pinshow 2000) and with it, its necessary correlate, the rate of dicted that (1) an increase in the rate of intake and the cor- gastrointestinal throughput of matter and energy (e.g., Mc- responding rate of gastric throughput would occur or (2) the Williams et al. 1999). However, recent studies have demon- gastric digestive efficiency would increase between the mid- strated that while large spare capacity may exist in some species nonbreeding and premigratory periods. Neither crude intake (reviewed in McWilliams and Karasov 2001), in species con- rate (the rate of intake calculated including inactive pauses; suming high inorganic and/or high protein content foods (e.g., Ϫ1 0.22 g DM [grams dry mass] or 3.09 kJ min ) nor the rate crustaceans or insects), the rate of intake can be limited by the Ϫ1 of gastric throughput (0.15 g DM or 2.85 kJ min ) changed rate of digestion (Zwarts and Dirksen 1990; Zwarts et al. 1996; over time. Gastric digestive efficiency did not improve between Klaassen et al. 1997; Gannes 2002). This lack of spare capacity the periods (91%) nor did the estimated overall energy assim- to intake rate may have important implications for the foraging ilation efficiency (63% and 58%, respectively). It was concluded strategies of these birds (e.g., time budget allocation, prey that the crustacean-dominated diet of the birds is processed at choice). Specifically, the presence of a digestive constraint (bot- its highest rate and efficiency throughout a season. It appears tleneck) may preclude an animal from increasing its energy that without a qualitative shift in diet, no increase in intake intake rate (e.g., before migration or in an anticipation of a rate is possible. Accepting these findings at their face value poses food shortage) via the mechanism of increasing the rate of food the question of how and over what time period the eastern consumption because the animal is forced to stop foraging curlews store the nutrients necessary for the ensuing long, while the food is being digested. How a digestively constrained northward nonstop flight. wild animal foraging under strict time limitation (e.g., tidal cycle) will cope with an increase in energy demand thus rep- resents an interesting life-history question that is addressed in this study. * Corresponding author; e-mail: [email protected]. The eastern curlew (Numenius madagascariensis) is a long- Physiological and Biochemical Zoology 76(5):704–715. 2003. ᭧ 2003 by The distance migratory shorebird spending the nonbreeding season University of Chicago. All rights reserved. 1522-2152/2003/7605-2141$15.00 on mudflats and estuaries of Australia (Lane 1987). Before This content downloaded from 23.235.32.0 on Wed, 4 Nov 2015 23:25:52 PM All use subject to JSTOR Terms and Conditions Digestive Inflexibility Limits Intake Rate in Eastern Curlews 705 northward migration to the coastline of East Asia and then to during the period of premigratory preparations as compared Siberia, the curlews have to build up nutrient stores sufficient with the mid-nonbreeding period. for a nonstop flight in excess of 5,000 km (Driscoll 1999). A It is important to stress that the study specifically investigated previous study (Y. Zharikov, unpublished data) demonstrated only gastric digestive performance (throughput rate and effi- that before migration, these birds prolonged their foraging to ciency). This is because the field nature of the study and meth- the maximum permitted by the duration of a low-tide period. ods employed allowed a precise measurement of only these At the same time, the proportion of time the birds spent inactive parameters of digestive physiology in wild individuals. None- was relatively high (34%–46%), and foraging was interrupted theless, data obtained in the process were sufficient to estimate every 5 min even though potential curlew predators were sel- in general terms seasonal trends in the overall digestive effi- dom present and prey were readily available. Both observations ciency and the rate of apparent metabolizable energy intake in are suggestive of a digestive bottleneck (e.g., Diamond et al. a wild population of curlews. 1986; Zwarts and Dirksen 1990). This study was designed to investigate the possibility of pre- Material and Methods migratory digestive modulation in a shorebird, the eastern cur- Study Area and Curlew Observations lew, foraging on abundant, high inorganic content prey (crabs and shrimp). First, we attempted to establish whether the rate The study was conducted on the western shore of North Strad- of food consumption in eastern curlews is indeed limited by broke Island, Moreton Bay, Queensland, Australia (27Њ25ЈS, the rate of digestion, as suggested by the earlier observations. 153Њ25ЈE) between November 18 and December 13, 2000, and In the field, the existence of such a constraint can be inferred February 5–22, 2001. Curlews depart from the study area by from an asymptotic relationship between the rate of intake mid-March, so these periods were defined as mid-nonbreeding achieved while actively foraging and the crude intake rate (the and premigratory, respectively. The specific study area repre- rate of intake calculated including periods of inactivity; e.g., sented a450 # 2,340 -m stretch of the intertidal zone occupied Zwarts 1990; Zwarts et al. 1996). An asymptotic relationship by ca. 100 eastern curlews. between these two rates implies that inactive pauses are nec- All eastern curlews observed in this study defended a roughly essary for (a part of) the digestive system to be cleared before rectangular segment of the unvegetated middle section of the foraging can resume (Diamond et al. 1986; Weiner 1992). It is mudflat between mangroves and sea grass beds. Although no also expected to occur when the rate of gastric throughput is birds were individually marked, the seasonally stable distri- plotted against intake rate achieved while actively foraging for bution of the individuals along the mudflat, their small home the same reason. A supplementary line of evidence suggesting range (!1 ha), and individual differences in behavior helped the existence of a digestive constraint can be obtained by plot- in avoiding repeated sampling of the same individuals within ting the crude rate of intake against the length of time available a period. To standardize for the environmental conditions ex- for foraging (Swennen et al. 1989). An assumption here is that perienced by the birds, all observations were carried out during a certain daily energy intake has to be achieved (e.g., Zwarts daylight hours, at clear to partially cloudy weather with no to et al.
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