OUP CORRECTED PROOF – FINALS, 12/10/2010, SPi CHAPTER 6 Cues and decision rules in animal migration Silke Bauer, Bart A. Nolet, Jarl Giske, Jason W. Chapman, Susanne Åkesson, Anders Hedenström, and John M. Fryxell Ice bars my way to cross the Yellow River , Snows from dark skies to climb the T’ai-hang mountains ! (Hard is the journey , Hard is the journey , o many turnings , And now where am I?) So when a breeze breaks waves , bringing fair weather, I set a cloud for sails , cross the blue oceans ! Li Po (701–762) ‘Hard is the journey’ Table of contents 6.1 Introduction 69 6.2 Challenges in migration 69 6.2.1 Where to go? 69 6.2.2 When to go? 69 6.2.3 Seasonal and life-cycle migration 70 6.2.4 Travel with or without a predefi ned target 70 6.2.5 Genetic or cultural transmission of migratory behaviour 70 6.3 Cues in the different phases of migration 71 6.3.1 Migration in plankton 71 6.3.2 Migration in insects 72 6.3.3 Migration in fi sh 74 6.3.3.1 Life-stage migration in Atlantic salmon 74 6.3.3.2 Feeding migration in pelagic fi sh: an undefi ned target 76 6.3.4 Turtle migration 77 68 OUP CORRECTED PROOF – FINALS, 12/10/2010, SPi CHALLENGES IN MIGRATION 69 6.3.5 Bird migration 78 6.3.6 Migration in mammals 81 6.3.6.1 Migration in bats 81 6.3.6.2 Migration in large herbivores 82 6.4 Discussion and Integration 84 6.1 Introduction reptiles, birds and mammals, and seek to identify the cues that are used for the different steps during The sheer beauty and impressiveness of animal each of their migrations. We fi nish by highlighting migrations have long puzzled observers and raised the general lessons that can be drawn from this the questions of how these animals fi nd their way, comparative study of cues and decision rules in what initiates their migrations and how they man- migration. age to schedule their journeys at apparently the right times. There are many challenges that animals face before and during migration, and they can be 6.2 Challenges in migration grouped into two major categories namely ‘where to 6.2.1 Where to go? go?’, dealing with orientation and navigation, and ‘ when to go?’, dealing with the timing of activities Going along a specifi c track requires cues for posi- and migration schedules. As these questions are tioning (navigation) and for fi nding the way fundamentally different, we also expect different towards the goal (orientation). Important cues for cues to provide relevant information. Furthermore, compass orientation include information from the animals make decisions in relation to their physio- magnetic fi eld, the Sun and the related pattern of logical state and therefore, cues can be further cate- sky light polarization and stars, while information gorized into internal and external signals. from, for example, landmarks and odours are used In this chapter, we tackle these questions not in for navigation. Excellent reviews on orientation and terms of why animals migrate (ultimate reasons), navigation can be found in, for example, Åkesson but how they make the right decisions before and and Hedenström (2007), and Newton ( 2008 ) . How- during migration (proximate factors). Migrating ever, for many migrating animals we still do not animals rely on external and internal information know how they fi nd their way, which orientation such that they can tune their behaviour to their and navigation abilities they have and which mech- (changing) requirements and to the development of anisms they use (e.g. Alerstam 2006 ; Holland et al . their seasonal environments. Here, we show that 2006b ) . these cues, defi ned as ‘signals or prompts for action’ ( Oxford English Dictionary ), are not well understood, 6.2.2 When to go? although they are most likely highly relevant both for advancing our fundamental understanding of Photoperiod has been shown to be involved in the migration and for increasing our capacity to man- timing of activities for many species, e.g. initia- age and conserve migratory systems under the ting ‘Zugunruhe’ (restless behaviour as the pre- threat of environmental change. migration phase starts) or determining the speed of In the following sections, we fi rst characterize migratory progression. This may come as no sur- migration from different perspectives, as different prise, as photoperiod is a reliable indicator of time migration types may require fundamentally differ- of the year and thus can be a useful predictor for the ent cues and decision rules. Thereafter, we intro- phenology of resources ( Fig. 6.1 ). Other local and duce migration in the major migratory taxa that are short-term factors infl uencing timing of migra- readily observable to biologists, i.e. insects, fi sh, tion include prevailing weather conditions, e.g. OUP CORRECTED PROOF – FINALS, 12/10/2010, SPi 70 CUES AND DECISION RULES IN ANIMAL MIGRATION Latitude daylight changes in the body plans often entail a habitat 0 hrs 60° N 2 change and therefore, internal signals are required 40° N 4 6 that are linked to these developmental processes as 20° N 8 well as cues to locate the next favourable habitat. 10 0° 12 However, these organisms may also live in seasonal 14 20° N 16 environments and, thus, the timing of ontogenetic 18 processes will also depend on the phenology of the 40° N 20 60° N 22 environment (Skelly and Werner 1990 ) . 24 JFMAMJJ A SON D Figure 6.1 Photoperiod, i.e. day length, as a function of latitude and 6.2.4 Travel with or without a predefi ned time of the year. Day length is here the time between dawn and dusk using target civil twilight (Sun 6° below horizon). The different shades of grey indicate the day length with darker colours depicting continuous light or permanent The best-known type of migration is that between a darkness (from Bauchinger and Klaassen 2005 ) . few specifi c localities, e.g. birds between wintering and breeding sites. In many cases, however, the migration does not lead to a specifi c locality or even temperature, wind, drought and precipitation, or to a certain more broadly defi ned area: In several water discharge in rivers, as these factors can sig- species of pelagic fi shes, both long-distance feeding nifi cantly infl uence the costs of the travel ahead and spawning migrations need not lead to a specifi c ( Chapters 4 and 5 ). target. Feeding migration is often driven by contin- There are also internal cues that serve as a clock uous local food search (Huse and Giske 1998 ; or time-keeping mechanism. Additionally, physio- Nøttestad et al . 1999) , while the return spawning logical state and developmental stage are important migration combines long-distance tracking of pre- cues as most migrants undergo morphological and ferred spawning sites with physiological constraints physiological changes in preparation for migration from swimming costs (Huse and Giske 1998 ; Slotte and internal signals, e.g. hormone levels, indicate and Fiksen 2000 ) . Although some large insect when these changes are completed ( Chapter 5 ). migrants, such as Lepidoptera (butterfl ies and moths) and Odonata (dragonfl ies) have regular, bi- directional seasonal long-distance migrations that 6.2.3 Seasonal and life-cycle migration involve movements that are directed in predictable We can distinguish between two life-cycle patterns ways but not targeted at a specifi c site or region in migratory animals. In one type, which includes (e.g. Chapman et al . 2008a , 2008b ; Wikelski et al . land reptiles, birds and mammals, most body trans- 2006 ) , most insect migrations do not even involve formations take place within the egg (reptiles and movements in consistent, seasonally preferred birds) or within the mother’s womb (mammals), directions. and the juveniles are only one or a few orders of magnitude smaller than the adult, and are generally 6.2.5 Genetic or cultural transmission well suited to the same environment as the adults. of migratory behaviour Migration in many of these animals is linked to a seasonal change in the environment and the cues How do offspring decide where and when to involved typically predict these changes. migrate? Migratory behaviour can be both geneti- The alternative pattern includes organisms with cally and culturally determined. In cultural trans- complex life-cycles, such as arthropods, fi sh, amphi- mission, the young copy their parents’ (or other bians and sea-reptiles, where animals spawn tiny group members’) behaviour. Consequently, species eggs that develop into individuals with a body size with culturally-transmitted migratory behaviour several orders of magnitude smaller than the adults, are expected to have a social life-style, longer life- and with a body form differing substantially from spans and (in higher vertebrates) extended parental the adult form. During development, the major care. Prominent examples include schooling fi shes OUP CORRECTED PROOF – FINALS, 12/10/2010, SPi CUES IN THE DIFFERENT PHASES OF MIGRATION 71 (e.g. the culturally-induced change of migration decision rules as their demands on the animal’s patterns and over-wintering sites in herrings; Huse physiology and behaviour differ. Similarities might et al . 2002 ), geese and swans among birds (e.g. Von exist across taxonomic groups in how animals deal Essen 1991 ) , and large herd-living mammals such with each of these steps but differences may also be as antelopes and wildebeest. expected depending on the specifi c way of migrat- Alternatively, migratory behaviour, e.g. routes, ing or their particular environment. threshold photoperiods, or preferred directions, can be genetically transmitted when there are no par- 6.3.1 Migration in plankton ents, peers, or elders—be it due to high mortality, short adult life-span, solitary life-style, absence of The annual or seasonal migrations in plankton parental care or separation of age classes, e.g.