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Behavioral Ecology Vol. 10 No. 1: 22-29
© 1999 International Society for Behavioral Ecology
Influences of parasites and thermoregulation on grouping tendencies in marine iguanas
Department of Animal Behavior, University of Bielefeld, Postfach 100131, D-33501 Bielefeld, Germany Max-Planck Institute for Behavioral Physiology, Abt. Wickler, D-82319 Seewiesen, Germany
Address correspondence to M. Wikelski, Department of Ecology, Ethology, and Evolution, 505 S. Goodwin Ave., University of Illinois, Urbana, IL 61801, USA.
Received 28 January 1998; accepted 28 April 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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I determined whether grouping behavior influences parasite load and body temperature of Galápagos marine iguanas, reptiles that rest gregariously. Mobile (or predatory) Ornithodoros ticks (4.7 mm average body length) approached at a ground speed of 65 cm/min and parasitized sleeping marine iguanas for 3.7 h per night, drawing about 0.1 ml blood. Contagiously transmitted Amblyomma ticks hang on to iguana hosts for days or weeks. Marine iguanas sleeping alone had 2.0 mobile ticks per night, while individuals sleeping in groups had 0.1 to 1.1 mobile ticks per night. Single iguanas decreased their mobile parasite load to 0.2 ticks per night by sleeping on bushes. Experimental nightly translocation of iguanas to areas without other sleeping iguanas significantly increased their mobile parasite burden above levels encountered by naturally single individuals (n = 4.6 ticks per night). Creating an experimental group of two animals reduced infestation with mobile ticks by 59% compared to levels on single animals. Over the course of weeks, mobile ectoparasite loads at grouping sites increased to levels found at single sites, at which point marine iguanas changed sleeping sites. Grouping had no effect on the prevalence of contagious ticks. Furthermore, grouping did not help to conserve body temperature in Genovesa iguanas, as measured by radiotelemetry. I conclude that marine iguanas group during daytime at microhabitats favored for thermoregulation (predation is absent in this population). Thermoregulation was not of prime importance for nightly aggregations, which instead served to reduce mobile ectoparasite load. As a minimum cost of infestation, I estimate that individuals sleeping alone would have a 5.4% lower annual energy budget due to tissue removal, not including potential internal infections.
Key words: body temperature, ectoparasites, grouping, iguanas, host-parasite interactions.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Marine iguanas are peculiar among reptiles for their gregariousness, which may result in enormous aggregations and even "piles" of individuals (Darwin, 1883)
. Two
hypotheses have been put forward to explain their active gregariousness:
(1) grouping at night has the thermoregulatory benefits of
"cuddling" (Boersma, 1982) and
(2) grouping into territories serves to avoid harassment during the breeding
season (Wikelski and
Bäurle, 1996). Here I evaluate
another factor that potentially influences grouping: parasite load
(Côté
and Poulin, 1995).
In most animal groups, individuals trade off the benefits of grouping
against its costs (e.g., Hamilton,
1971; Magurran,
1990; Strassmann,
1992; Wittenberger and Hunt,
1984). Two of the most important benefits in groups are increases
in vigilance and numeric dilution. Both factors reduce the chances that
individual group members will suffer fitness losses due to predation (for a
review, see Krebs and Davies, 1993).
However, large groups are more conspicuous and may therefore attract more
predators (e.g., for primates see Noe and Bshary,
1997). This logic can be extended to "micropredators,"
the ubiquitous parasites of animals. Parasite prevalence often constitutes a
cost of living in groups (e.g.,
Côté
and Poulin, 1995; Kunz,
1976; Mooring and Hart,
1992; but see Arnold and
Lichtenstein, 1993). The mechanism behind this cost is that
parasite transmission from one individual to the next is facilitated when
animals are in closer contact, as are grouped individuals compared to single
individuals. In a meta-analysis,
Côté and Poulin
(1995) confirmed the expected positive
correlation between host group size and both prevalence and intensity of
contagious parasites. There was no effect of host group mobility on the
strength or direction of these relationships. However, this positive
correlation between group size and infestation prevalence only held for
contagious, or nonmobile (sensu
Côté
and Poulin, 1995), parasites. Mobile, or predatory, parasites, on
the other hand, usually infected grouping individuals in smaller numbers than
they did single individuals
(Côté
and Poulin, 1995).
Here I determined the effect of grouping in marine iguanas on the
prevalence of two types of parasites, one sedentary (permanently attached to
hosts) and contagious (sensu
Côté
and Poulin, 1995), the other mobile and predatory, parasitizing
hosts only during the night (see below for details). I used obvious and highly
abundant ectoparasites of marine iguanas, the ticks Amblyomma spp.
(sedentary) and Ornithodoros spp. (mobile; see
Gadsen and Guerra, 1991;
Keirans et al., 1973,
1980;
Kohls et al., 1969). My aim was to
quantify the prevalence of parasites for individuals sleeping in groups versus
those that sleep singly. I also experimentally manipulated this situation to
avoid possible effects of interindividual differences in parasite avoidance or
resistance. To assess the costs of the parasite burden, I provided an analysis
of the energetic costs suffered by parasitized individuals. As an alternative
explanation for nightly groupings in marine iguanas, I considered
thermoregulatory "cuddling" for warmth. Boersma
(1982) suggested that marine iguanas on
Fernandina island in the Galápagos archipelago
group and establish body contact to conserve heat during the night.
Natural history of the host
Marine iguanas are ubiquitous along the rocky shores of the
Galápagos Islands and can occur in densities
as high as 8000 individuals per km coastline (Laurie,
1989; but see Cayot et al.,
1994). There are three types of aggregations that may be
formed: (1) after foraging in intertidal areas, marine iguanas may
temporarily congregate along the coast at sites suited for thermoregulation
(Buttemer and Dawson, 1993;
Trillmich and Trillmich, 1986;
Wikelski and Trillmich, 1994). I did not
investigate this behavior here; (2) toward the late afternoon,
individuals may congregate at sites relatively close to the coast. This mode
of aggregation is especially prevalent in the larger individuals of a
population, which often position themselves somewhat symmetrically like the
spokes of a wheel (Boersma 1982). In these
aggregations, individuals may also pile on top of each other, and may or may
not stay throughout the night; (3) toward dusk, most individuals retreat
from the coast to rest either in crevices, caves, below bushes, or in lava
cracks. Individuals may also pile up in these nightly aggregations.
Predation pressure is largely absent for marine iguanas above hatchling
size. The only exception are nesting females, which fall prey to the
Galápagos hawk
(Laurie and Brown, 1990). This, however,
happens only during daytime, during specific times of the year, and at areas
usually far off the coastal sleeping sites (Wikelski M, personal observation).
Furthermore, hawks are absent on Genovesa island and thus predation can be
excluded as a selective force influencing grouping during my study.
Marine iguana parasites
Marine iguanas suffer ectoparasitism from at least three groups of ticks.
The most prominent ticks are the black, round Amblyomma darwini and
Amblyomma williamsii (Bequaert,
1932; Hirst and Hirst,
1910; Schatz, 1991).
Darwin's ground finches (Geospizae spp.) are known to remove those
ticks occasionally, although marine iguanas lack a pushup body posture which
aids cleaning birds in removing ticks (but see
Galápagos land iguanas and
Galápagos land tortoises;
Carpenter 1966). Nymphs of
Amblyomma species reside in skin folds along the neck of marine
iguanas. Adult Amblyomma ticks are mainly found on ventral parts of
marine iguanas, especially at the soft tissues of the cloaca, where they hang
on for several days to weeks. It is unknown what determines infestation
duration. From what little is known about the ecology of these ticks, they are
presumably contagiously transferred between individual hosts
(Schatz, 1991, personal
communication).
The second, less conspicuous group of parasites consists of
Ornithodoros darwini and O. galapagensis ticks, which only
infest marine iguanas at night or when the iguanas are in crevices.
Ornithodoros spp. fill with blood in a few hours. Both species are
Galápagos endemic and were first described
about 30 years ago (Kohls et al., 1969).
They occur on at least eight Galápagos islands
(Gadsen and Guerra, 1991;
Keirans et al., 1980). O.
galapagensis outnumbers O. darwini by far and is mainly
associated with marine iguanas. The only other Ornithodoros species
in Galápagos is O. near
denmarki, a parasite of marine birds. Of the approximately 100
species in the genus Ornithodoros, only 4 are host specific to
reptiles; 56% parasitize cave-dwelling bats, 20% infest
birds nesting in rocks and caves, and another 20% infest mammals.
Although nearly 90% of Ornithodoros species are restricted to
the Western Hemisphere, some species are truly cosmopolitan on marine birds,
swifts, and swiftlets (Keirans et al.,
1980). It is unclear how important marine iguanas are as
mating-encounter sites for ectoparasites (Yuval,
1994).
A third group of marine iguana parasites, which I do not consider here, are
three species of Vatacarus ticks living in the nasal fossae
(Schatz, 1991). In this study I
concentrate on the northeastern-most population of marine iguanas on Genovesa
Island, which has the smallest adult body sizes of all marine iguana
populations (Rassmann et al., 1997;
Wikelski and Trillmich, 1997;
Wikelski et al., 1997). Nevertheless, all
of the above-mentioned parasites, especially Ornithodoros spp., have
also been found in other island populations of marine iguanas
(Keirans et al., 1980; Wikelski M,
unpublished data).
Marine iguanas have no malarial infections (Wikelski M, unpublished data),
and there is no information on other bloodborne diseases or parasites. There
were no coccidial infections in 128 marine iguanas from different islands
(Couch et al., 1996).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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I studied marine iguanas at the "Salvaje de Corazon" site on Genovesa Island (89°59' W, 0°19' N) from 1 November 1992 until 3 March 1993. This period experienced a long-term El Niño, during which environmental conditions were unusually hot and moist (Wikelski and Trillmich, 1997)
.
Body temperatures of marine iguanas were measured either by inserting a
fast-acting thermoprobe deep into the cloaca of individuals or by
radiotelemetry (see Wikelski and Trillmich,
1994, for details). I implanted 20 animals with radio thermistors,
which transmitted body temperatures for 14-90 days. Operative environmental
temperatures were measured radiotelemetrically by monitoring temperature
inside a black copper ball (15 cm diam; see
Bakken, 1992;
Wikelski et al., 1996. To evaluate
temperature differences between sites, I recorded temperature within two
copper balls simultaneously. To compare operative temperatures inside and
outside of beach piles, I mounted each copper ball on a 4-m long bamboo pole
and put one into the presumed center of the pile, while the other was placed
approximately 1.5 m away. Animals did not react to this treatment if it was
performed extremely slowly and carefully.
The effect of piling on body temperature was directly evaluated by measuring body temperature changes over a 4h period from 1730 h to 1930 h to 2130 h. I only used data on body temperature change when two conditions were met: (1) two animals with implanted thermotransmitters had joined the same pile location (within a radius of 50 cm) before 1730 h and (2) one of those animals touched other animals in the pile with at least half of its body, while the other animal was not touching other animals (except with its foot or its tail). Thus, one animal was piling, the other one not, but both experienced a similar microclimate. Seven such instances for different combinations of implanted individuals could be recorded.
I conducted observations on the prevalence of both Ornithodoros
and Amblyomma spp. after sunset. I combined the two sets of
congeners, Ornithodoros darwinii and O. galapagensis, as
well as Amblyomma darwinii and A. williamsii, respectively,
into two ecological species groups. This seems justified by the fact that
hybridization between congeneric tick species may occur
(Guglielmone and Mangold, 1993) and by
the respective morphological and ecological similarities of each congeneric
pair (see Verdammen-Grandjean, 1966).
Nothing is currently known about the ecology of either
Galápagos tick genus, but in a closely related
Peruvian seabird tick (O. amblus), females lay about 450 eggs, and
the life cycle is completed in 63 to 401 days. Adult O. amblus also
only feed for short periods (15-55 min.;
Clifford et al., 1980;
Khalil and Hoogstraal, 1981). Unfed
adults of other closely related species can survive for many years
(Anastos, 1957).
Marine iguanas went to sleeping places before sunset and moved little at
night, except for occasional leg and tail movements in what appeared to be
active sleep phases (Wikelski M, unpublished data; for behavioral data
on sleep phases in lizards, see Ayalaguerrero and
Huitronresendiz, 1991). Therefore, I assumed that the observed
sleeping aggregations were stable throughout the night. Iguanas were not
active at night; thus nightly groupings were presumably not primarily
influenced by mating decisions (see Wikelski et al.,
1996). I considered individuals as grouped if four or more
individuals were resting within half a body length of each other. A
"pile" of iguanas is defined as individuals touching the body of
another animal with at least one third of their own body.
To conduct observations and parasite counts, groups of sleeping iguanas were approached by a single observer who either used moonlight or the darkened light of a flashlight for vision. The total number of group members was counted. In several cases individuals sleeping in groups were touching each other. As a conservative (tick-centered) estimate of "apparent" group size, I used only the approximate surface area of an individual to determine the number of individuals per group (e.g., if half the individual was covered by another animal, I counted it as 0.5 individual only; final group numbers were rounded to the nearest integer number). This measure accounted for the reduced surface area suitable as attachment site for ectoparasites. In only a few cases were individuals entirely covered by one or two other individuals. In these cases, I did not count the covered animals as group members, since covered animals were not found to be infested by Ornithodoros ectoparasites in control counts. However, covered individuals were parasitized by Amblyomma ticks. This apparent group size is a conservative measure of infestation rate compared to including covered individuals; the latter would make the differences between group and single individuals even more pronounced. I used the same measure of apparent group size for Amblyomma and Ornithodoros ticks. Infestation rate is defined as the total number of ticks found in a group divided by the number of group members. On 23 January 1993, all iguanas sleeping in 10 groups throughout the study area were counted and their Ornithodoros and Amblyomma parasite burden investigated after midnight. This count provided an independent determination of group size on infestation rate. I refer to the "start" of a new group if I found a group of sleeping iguanas at a site where I had not seen iguanas sleeping during the preceding week. The "break up" of a group was defined when fewer than four iguanas were found sleeping at a site that was occupied by a sleeping group during the preceding 3 weeks.
I found Ornithodoros. spp. preferentially located on the dorsal parts of animals, although I initially searched all parts of individuals carefully for the occurrence of ticks. The preferred infestation sites appeared to be the tail vein and the dorsal spine vein, where about 90% of ticks were located. The remainder were distributed at femoral veins and the flanks of animals. Only Ornithodoros ticks > 2 mm carapace length were found to infest iguanas at night.
In contrast, Amblyomma spp. were distributed almost exclusively on the ventral part of the body of hosts, except for the nymphs, which infest the host around its skin folds at the neck. I only included Amblyomma individuals > 2 mm body length in the counts. I did not want to disturb nightly groupings, thus I could not check for Amblyomma ticks in the same groups in which I counted Ornithodoros ticks (because of the ventral attachments sites of Amblyomma spp.). Therefore, I used adjacent groups of similar size to count Amblyomma ticks during the same nights. Marine iguanas at my study site were not awakened or otherwise disturbed by these observations.
Walking speeds of each 10 Ornithodoros and Amblyomma ticks were measured in empty (presumably hungry) ticks in the shade of a tent. Ticks were set on a 2-cm wide runway consisting of a calibrated driftwood board of 30 cm length with side walls of 3 cm height. The ticks were stimulated with a pen held behind them (simulating a bird's beak) to run at least 20 cm. The time taken for this exercise was measured with a wrist watch.
To determine the amount of blood extracted from the host, 11 Ornithodoros ticks were collected after they naturally left their respective host, and 11 Amblyomma ticks were actively removed from their hosts when they appeared full of blood. Their full body volume was measured to the nearest 0.01 ml by submersion in water. Thereafter, ticks were killed and gut contents measured.
Experimental manipulations
I carefully picked up 10 nonparasitized individuals from nonfocal groups
between 2000 h and 2200 h, covering the iguanas' eyes with one hand and the
head with the other hand. When done extremely carefully, other group members
were not affected by the removal of a conspecific. Thereafter, animals were
translocated to different places in the study site. I placed animals on the
ground and again held my hand above their head for approximately 5-10 s until
the animals stopped moving and continued to rest or sleep. To create eight
experimental groups of two, this procedure was repeated twice, and a second
animal of similar body size was placed within one body length distance of the
first experimental individual. After an initial test trial period, all
translocated animals except one remained sleeping throughout the night at the
new place. One iguana woke up and left and was therefore discarded from the
analysis. The Ornithodoros infestation of experimental animals was
checked every half hour throughout the night until 0400 h, when
Amblyomma ticks were also counted. The maximum number of ticks was
found between midnight and 0200 h and usually did not show any changes between
these two sampling points. Only the maximum number of ticks per animal and
night was used for the analysis. During these experiments I also determined
the attachment duration to the nearest half hour by marking the first and last
appearance of an individual tick on a host.
Statistical analysis
I analyzed data using SPSS (1991) for
Windows; means ± SD are given unless otherwise noted. Error
estimates in regression equations are given as means ± SE. Two-tailed
tests were used and the 
level was set at 5%. Data from natural
and experimental situations were compared using ANOVA.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Parasites and infestation rates
Both Amblyomma and Ornithodoros ticks moved relatively fast over a plain surface (Table 1; total body lengths of measured individuals about 4 mm, ambient temperature about 33°C; Mann-Whitney U test, N1,2 = 11, p >.05). On average, adult Ornithodoros ticks were about 40% larger and had about 50% larger gut volumes compared to Amblyomma ticks (for both cases: Mann-Whitney U test, N1,2 = 11, p <.001). While Ornithodoros spp. attached only at night for several hours, Amblyomma spp. infested hosts for days (Table 1). Ornithodoros ticks attached to hosts between 1900 h and 2300 h, and the last ticks left their hosts at 0430 h.
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Mean group size of all marine iguana groups sampled on 23 January 1993 was 29.7 ± 27.4 individuals (n = 10 groups). The infestation rates per individual were initially low but increased over time when animals were using the same sleeping location. When animals appeared at a new sleeping site, the infestation rates were initially moderate and declined as more and more animals joined the sleeping aggregation. However, after about 3 weeks, infestation rates increased again. This observation was qualitatively repeated twice (Figure 1).
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Ornithodoros infestation rates were influenced by group size, but Amblyomma infestation rates were not. Ornithodoros infestation rates were lowest in individuals sleeping in groups or singly in bushes (Figure 2). There was a significantly higher prevalence of ticks when individuals were sleeping alone on rocks than when they slept in groups or in bushes. The prevalence of Ornithodoros ticks in single experimental individuals was significantly higher than in any other treatment group (ANOVA, F5,57 = 12.8, p <.001; followed by post-hoc least-significant difference tests; see Figure 2 for differences between groups). However, there was no significant difference in Amblyomma tick infestation rate between any of the treatment groups (ANOVA, ns).
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To analyze the influence of grouping on infestation rate, I determined the slope of the regression of the total number of parasites against the apparent number of individuals in a group (Figure 3). A slope of 1 would indicate that the average number of parasites per host is constant, while a slope below 1 would indicate a decrease of infestation rate with group size. The total number of Ornithodoros ticks increased with group size by a factor of 0.27 [linear regression: total Ornithodoros ticks in group = 7.8 (±4.1) + 0.27 (±0.10) x individuals in group; F1,10 = 6.7, p =.03, R2 =.46]. Therefore, individuals in larger groups had lower Ornithodoros infestation rates per individual than individuals in smaller groups. Infestation by Amblyomma ticks, on the other hand, did not change with group size, as indicated by a regression slope of close to 1.0 [linear regression: total Amblyomma ticks in group = 6.7 (±7.1) + 0.86 (±0.18) x individuals in group; F1,10 = 23, p =.001, R2 =.74; other regression models did not fit better than a linear one]. To investigate whether parameters other than average number of ticks per iguana may relate to group formation, I determined the variance in number of parasites per iguana in relation to group size. The variance in Ornithodoros infestation declined with group size [a logarithmic model fitted significantly better than a linear one: logarithmic regression: y = 1.57 (±0.35) - 0.33 (±0.11) ln (x); F1,8 = 8.6, p =.01, R2 =.51). In contrast, there was no change in variance in Amblyomma infestation with group size [linear regression: y = 0.47 (±0.18) + 0.0 (±0.0) x, F1,8 = 0, p =.95, R2 = 0).
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Body temperature and nightly grouping
To determine whether grouping affected nighttime body temperature, I
considered, as two alternatives, whether the grouping site per se affected
body temperature and whether "cuddling"
(Boersma, 1982) affected body temperature.
These measurements were conducted after the reproductive season, in February
and March 1993.
Site effects
First, I determined whether marine iguanas sleeping alone in crevices or
cracks (usually 20-50 m off the coast) could achieve similar nighttime body
temperatures to individuals sleeping in beach piles (usually found very close
to the coast, as described by Boersma,
1982). This tests for the effect of sleeping site selection on
nightly body temperature. I found that individuals of all body sizes achieved
considerably higher body temperatures in crevices compared to beach piles
(mean differences in body temperature between crevice and beach
individuals: 0.72 ± 0.64°C; Wilcoxon test, df = 15
individual pairs of similar body sizes measured during 15 nights at 2000 h,
Z = -3.1, p =.002). This effect was corroborated by
measuring standard operative temperature at those places at about 2000 h.
Operative temperature was always higher around crevices than at beach piling
sites (28.8° ± 3.1°C versus 27.7° ± 2.5°C, same
setup as above: Wilcoxon test, df = 15, Z = -3.2, p
=.001). Furthermore, there was always a higher standard operative temperature
inside as compared to 1.5 m outside of the pile location (mean difference in
temperature was 1.61° ± 0.65°C, Wilcoxon test, df = 8 pile
locations on 8 days, Z = -2.5, p =.01).
"Cuddling" effects
If piling conserves body temperatures in iguanas, I expected to find higher
body temperatures in piled than in single individuals at the same site after
the same sleeping duration. In a repeated-measures ANOVA I determined whether
there were differences in the body temperatures at three different times (1730
h, 1930, 2130 h) between piling versus nonpiling individuals while correcting
for their respective body masses (330-720 g) as a covariate. I did not find
any significant difference in body temperature change over time between piling
and nonpiling marine iguanas (repeated-measures ANOVA with mass and day of
measurement as covariates, F2,14 = 0.01, p
=.96; for mass, p =.18, for date, p =.46; higher
level interactions were not significant).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Observational and experimental data showed that grouping of the host reduced the infestation rate by mobile, but not by contagious, ectoparasites. Because the numbers of mobile parasites increased at sleeping locations over time, hosts shifted their sleeping locations and thus ensured a low infestation rate. Singly-sleeping iguanas encountered lowest infestation rates at places that were hard for the investigated parasites to access, on bushes. Sleeping in groups did not influence body temperature of Genovesa Island marine iguanas.
Ecology of parasitic ticks
Amblyomma spp. and Ornithodoros spp. were the most
commonly observed groups of macroscopically visible parasites on marine
iguanas (Keirans et al., 1980;
Kohls et al., 1969). They belong to the
88 known species of 14 families of Galápagos
Acari (Schatz, 1991).
Although ticks are usually considered "contagious" parasites
(sensu
Côté
and Poulin, 1995), this infestation mode only describes the
situation in Amblyomma ticks. Amblyomma darwini and A.
williamsi stay firmly attached to the host for at least several days if
not weeks. These parasites seem astonishingly unaffected by the hosts'
prolonged foraging and diving bouts in the sea
(Carpenter, 1966). The fast speed of
ground movement (about 50 cm/min.) enables these ticks to switch easily
between hosts resting adjacent to each other, making a contagious infestation
possible (see also, e.g., Kunz,
1976).
Although Ornithodoros ticks achieve similar ground speeds, they seem to have adopted a generally much more mobile, or predatory, way of life. In this study Ornithodoros spp. were only observed to ambush marine iguanas at night. The spatial distribution of Ornithodoros ticks demonstrated by my experimental study seemed to resemble an equal distribution along the habitat, at least for the habitat suitable as marine iguana nightly resting sites.
A clear distinction between the two types of ticks is the attachment site
on the host. Amblyomma is confined to the neck skin folds as nymphs
and mostly to the ventral body parts as adults, whereas Ornithodoros
infests mostly the dorsal and tail parts of marine iguanas. It appears that a
niche segregation along a host's body is common in ectoparasites, but the
reasons for this are generally not well understood
(Chilton et al., 1992b).
The most striking difference between the two marine iguana ticks, however,
is the duration of attachment on the host. While Amblyomma
individuals stay attached for at least several days, Ornithodoros
individuals fill up within hours and thereafter leave to retreats between
rocks (for related cases, see Chilton et al.,
1992a; Matuschka et al.,
1990a, b). However, it is not
known if Amblyomma ticks slowly draw blood during the entire
attachment duration or if the prolonged attachment duration serves other
functions. For example, it could be important for reproduction. We currently
lack information on the reproductive ecology of both Amblyomma and
Ornithodoros ticks to answer this question.
Host-parasite interactions: why group?
So far, it has been suggested that marine iguanas group either at night for
the thermoregulatory benefits (Boersma,
1982) or that grouping during daytime helps to avoid harassment in
a reproductive context (Wikelski et al.,
1996). During the present study, only nonreproductive groupings
were investigated, even though the study also covered the reproductive period
(December).
Nonreproductive grouping has so far been attributed solely to the
thermoregulatory benefits (Boersma, 1982).
However, Boersma could not measure the body temperature of individuals as they
joined the pile, nor did she measure the standard operative environmental
temperature at the site of piling versus the sites where single iguanas were
sleeping. My radiotelemetry data showed no effect of pilling versus single
sleeping on the rate of body temperature change; thus there was no
benefit of "cuddling" in my population. However, marine iguanas on
Genovesa have about seven times smaller body masses than the animals
investigated by Boersma (1982) on
Fernandina. It could therefore be argued that a cuddling effect found in piles
of large iguanas might not be detectable in piles of small marine iguanas, due
to a different surface-to-volume ratio (e.g.,
Schmidt-Nielsen, 1984).
A more likely explanation for the formation of beach piles is that iguanas
gather at spots that offer a slightly better (i.e., warmer) microclimate
during the late afternoon hours, when piles usually develop. This was
supported by the measurements of standard operative environmental temperature
(after Bakken, 1992), which were always
slightly higher at places where iguanas piled. Circumstantial evidence also
shows that iguanas often left those beach piles shortly before sunset only to
join conspecific groups farther off the coast
(Wikelski and Hau, 1995; Wikelski
M, personal observation). This supports the view that the direct
thermoregulatory benefits at piling sites are only short lived, as they may
only exist during the afternoon hours, For sleeping, iguanas may then search
for the warmer sites farther inland.
In addition to possible thermoregulatory reasons for grouping, there seemed
to be a clear effect of grouping on parasite load, in that individuals in
groups were less parasitized by mobile Ornithodoros ectoparasites
(see Poulin and FitzGerald, 1989).
Furthermore, the variance in infestation rates was less in larger groups of
iguanas. In contrast, the infestation rate by contagious parasites and its
variance appeared unaffected by these behavioral decisions of the hosts. The
likely reason for this difference was that contagious, fast-moving parasites
could switch hosts at any time whenever hosts rested close to each other. It
is unclear if individual behavioral variation in the host (e.g., the high
sleeping/resting site fidelity) influences Amblyomma infestation
pattern.
Taken together, it appears that marine iguanas group during daytime at
places favored for thermoregulation. These may be either relatively cool
microhabitats during the heat of the day (e.g., the shade of an observational
chair, as seen in the present study) or relatively warm habitats during the
late afternoon hours (e.g., places at the beach). It is conceivable that
already resting individuals are used as "thermal indicators" for
suitable areas by passing iguanas. This would explain the attraction of
iguanas to model iguanas during the nonreproductive season, which we found
during a previous study (Wikelski et al.,
1996). The nightly groupings might be influenced both by
microhabitat selection and parasite avoidance strategies. Marine iguanas that
rested in groups moved to alternative grouping sites when parasite infections
surged at "traditional" sleeping sites (for similar effects in
primates, see Freeland, 1976). This
situation parallels the bat fly infections of bats roosting in caves
(Kunz, 1976). In all these cases,
parasites presumably located persistent piles or groups of hosts.
The pattern of ectoparasitism in marine iguanas confirms a meta-analysis on
sociality and parasitism.
Côté and Poulin
(1995) suggested that parasites have the
potential to select for either larger or smaller group sizes, or for solitary
individuals, depending on their mode of infestation. In their analysis of 15
host-parasite systems (5 birds, 7 mammals, and 3 fish), the direction of
selection pressure on the host depended mostly on the lifestyle of the
parasites. Contagious parasites were more prevalent and intense in larger host
groups. In contrast, mobile parasites decreased with increasing host group
size. My data on marine iguana ectoparasitism demonstrate that only one
effect, the decrease in mobile parasites, occurred within this host. My data
corroborate the notion that closely related ectoparasites can have different
life-history modes and may thus affect host behavior differently (see
Poulin, 1994).
The gregariousness during the iguana mating season and a possible
temperature/infestation trade-off indicate that there are (seasonally)
differing reasons for groupings (cf. Mooring and
Hart, 1992; Packer et al.,
1990; Underwood, 1982).
It is currently unclear whether (ecto-) parasites have any influence on
grouping in other iguanids (see, e.g., Burghardt and
Rand, 1985).
Does infestation affect iguana fitness?
There is widespread evidence for costs of ectoparasites to hosts (e.g.,
Duffy, 1983;
Richner et al., 1993; see also
Hart, 1990). Ticks may transmit blood
parasites such as Rickettsia-like blood cell inclusions
(Schall, 1990). Blood parasites or a
combination of ectoparasites and blood parasites reduced the hemoglobin
content in lizards, and consequently maximum oxygen consumption dropped by
15%. Running stamina was found to decrease by up to 20%, which
would imply a reduced ability to maintain territories
(Schall, 1990;
Schall et al., 1982; see also
Sorci et al., 1996). Tail regeneration
was reduced in parasitized Lacerta lizards
(Opplinger and Clobert, 1997). There were
also hormonal alterations in lizard hosts caused by parasites
(Dunlap and Schall, 1995). These might
increase the host's susceptibility to even larger numbers of ectoparasites
(Salvador et al., 1996).
On the other hand, Bull and Burzacott
(1993) did not find a fitness effect of
tick load on Australian sleepy lizard hosts (these skinks have similar adult
body masses as marine iguanas on Genovesa Island, 500-700 g). Nevertheless,
there was at least an energetic cost of infestation because an adult tick
engorges up to 0.5 ml blood (Chilton and Bull,
1993). Furthermore, parasite effects on fitness were only
investigated by correlations, and the authors suggested that only an
experimental manipulation would reveal any real effect on individuals
(Bull and Burzacott, 1993). Dunlap and
Mathies (1993) demonstrated a direct
effect of ectoparasites by showing that tick-infested Sceloporus
lizards had lower hematocrits and possibly much reduced aerobic capacities as
compared to non-infected individuals.
In marine iguanas it could not be quantified if infested individuals suffer
costs and, for example, mount an immune response to ticks. It is possible that
at least Amblyomma ticks are largely benign, especially because
iguanas show no obvious behaviors to avoid infestation. However, the
behavioral changes in marine iguanas related to the infestation by mobile
Ornithodoros ectoparasites make at least some cost of infestation
likely. An immediate cost of ticks, even in the absence of disease
transmission, would be the removal of tissue (blood). An iguana that always
rests alone would suffer infestation of 723 Ornithodoros ticks per
year (1.98 ticks x 365 nights), whereas it would only host 219 ticks
(0.6 ticks x 365 nights) if it were sleeping in a group every night of
the year. Assuming a mean blood removal per Ornithodoros tick (0.114
ml) and tissue production (or growth) efficiencies of 75%
(Baxter, 1989;
Prosser and Brown, 1965), this amounts to
an 82.4 ml blood loss, or approximately 549 kJ energy loss per year for a
singly-sleeping versus 23.7 ml blood loss or 157 kJ energy loss per year for a
group-sleeping individual. This represents 7.5% versus 2.1% of the
annual energy budget for a medium-sized Genovesa marine iguana (300 g) of 7300
kJ (20 kJ x 365 days; cf. Drent et al., submitted;
Nagy and Shoemaker, 1984;
Wikelski et al., 1997). It appears likely
that the difference of 5.4% in the annual energy balance between
grouping and nongrouping individuals selects for the observed behavioral
differences in host grouping behavior.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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I thank E. Connors, A. Türk, B. Gall, M. Hau, and S. Bäurle for invaluable field asisstance; the Galápagos National Park Service, the Charles-Darwin Research Station, and Metropolitan touring through the yacht ISABELA II and TAME for enabling this work; and E. Ott and S. Layer for providing communication; M. Hau, F. Trillmich, H. Schatz, H. Snell, N. Hillgarth, and two anonymous reviewers for comments improving previous versions of the manuscript. Special thanks to W. Wickler, Max-Planck Institut für Verhaltensphysiologie, and Fritz Trillmich, University Bielefeld, for continuing support. This is contribution no. 577 of the Charles Darwin Foundation and was supported by a Feodor-Lynen and a Smithsonian Tropical Research Institute fellowship and the DFG grant Tr 105/7 to Fritz Trillmich.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Anastos G, 1957. The ticks or Ixodides of the U.S.S.R. A review of the literature. Publication 548. Washington, DC: U.S. Public Health Service.
Arnold W, Lichtenstein AV, 1993. Ectoparasite loads
decrease the fitness of alpine marmots (Marmota marmota) but are not
a cost of sociality. Behav Ecol
4:36-39.
Ayalaguerrero F, Huitronresendiz S, 1991. Sleep patterns in the lizard Ctenosaura pectinata. Physiol Behav 49:1305-1307.[Medline]
Bakken GS, 1992. Measurement and application of operative and standard operative temperatures in ecology. Am Zool 32:194-216.
Baxter KL, 1989. Energy metabolism in animals and man. Cambridge: Cambridge University Press.
Bequaert J, 1932. On the ornate nymphs of the tick genus Amblyomma (Acarina: Ixodidae). Z Parasitenk 4:776-783.
Boersma PD, 1982. The benefits of sleeping aggregations in marine iguanas (Amblyrhynchus cristatus). In: Iguanas of the world (Burghardt GM, Rand AS, eds). Park Ridge, New Jersey, Noyes Publishing; 292-300.
Bull CM, Burzacott D, 1993. The impact of tick load on the fitnes of their lizard host. Oecologia 96:415-419.[Web of Science]
Burghardt GM, Rand AS, 1985. Group size and growth rate in hatchling green iguanas (Iguana iguana). Behav Ecol Sociobiol 18:101-104.[Web of Science]
Buttemer WA, Dawson WR, 1993. Temporal pattern of foraging and microhabitat use by Galápagos marine iguanas, Amblyrhynchus cristatus. Oecologia 96:56-64.[Web of Science]
Carpenter CC, 1996. The marine iguana of the Galápagos Islands, its behavior and ecology.Proc Calif Acad Sci 34:329-376.
Cayot LJ, Rassmann K, Trillmich F, 1994. Are marine iguanas endangered on islands with introduced predators? Notic Galapag 53:13-15.
Chilton NB, Andrews RH, Bull CM, 1992a. Interspecific differences in the movements of female ticks on reptiles. Int J Parasitol 22:239-242.[Web of Science][Medline]
Chilton NB, Bull CM, 1993. Oviposition by two Australian species of reptile tick. Acarology 34:115-121.
Chilton NB, Bull CM, Andrews RH, 1992b. Niche segregation in reptile ticks: attachment sites and reproductive success of females. Oecologia 90:255-259.[Web of Science]
Clifford CM, Hoogstraal H, Radovsky FJ, Stiller D, Keirans JE,1980 . Ornithodoros (Alectorobius) amblus (Acarina: Ixoidea: Argasidae): identity, marine bird and human hosts, virus infections and distribution in Peru. J Parasitol 66:312-323.
Côté IM, Poulin R, 1995. Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159-165.[Abstract]
Couch L, Stone PA, Duszynski DW, Snell HL, Snell HM,1996 . A survey of the coccidian parasites of reptiles from islands of the Galápagos archipelago 1990-1994. J Parasitol 82:432-437.[Medline]
Darwin C, 1883. Journal of researches, new ed. New York: Appleton.
Duffy DC, 1983. The ecology of tick parasitism on densely nesting Peruvian seabirds. Ecology 64:110-119.[Web of Science]
Dunlap KD, Mathies T, 1993. Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards.Copeia 1993:1045-1048.
Dunlap KD, Schall JJ, 1995. Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 68:608-621.[Web of Science]
Freeland WJ, 1976. Pathogens and the evolution of primate sociality. Biotropica 8:12-24.
Gadsen H, Guerra G, 1991. Loc acaros ectoparasitos de Amblyrhynchus cristatus Bell (Sauria: Iguanidae) como trazadores zoogeograficos, en las islas Galápagos, Ecuador. Folia Entomol Mexicana 83:183-197.
Guglielmone AA, Mangold AJ, 1993. Cross-mating between Amblyomma parvum Aragao 1908 and Amblyomma pseudoparvum Guglielmone Mangold et Keirans 1990 Acari Ixodidae. Folia Parasitol 40:144-145.
Hamilton WD, 1971. Geometry of the selfish herd.J Theor Biol 31:295-311[Web of Science][Medline]
Hart BL, 1990. Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav Rev 14:273-294.[Web of Science][Medline]
Hirst S, Hirst LF, 1910. Description of five new species of ticks (Ixodidae). Ann Magaz Nat Hist 4:299-308.
Keirans JE, Clifford CM, Hoogstraal H, 1980. Identity of the nymphs and adults of the Galápagos iguanid lizard parasites, Ornithodoros (Alectorobius) darwini and O. (A.) galapagensis (Ixodoidea: Argasidae). J Med Entomol 17:427-438.[Web of Science]
Keirans JE, Hoogstraal H, Clifford CM, 1973. The Amblyomma (Acarina: Ixodidae) parasitic on giant tortoises (Reptilia: Testudinidae) of the Galápagos islands. Ann Entomol Soc Am 66:673-688.
Khalil GM, Hoogstraal H, 1981. The life cycle of Ornithodoros (Alectorobius) amblus (Acari:Ixoidea: Argasidae) in the laboratory. J Med Entomol 18:134-139.[Web of Science]
Kohls GM, Clifford CM, Hoogstraal H, 1969. Two new species of Ornithodoros from the Galápagos islands (Acarina: Argasidae).J Med Entomol 6:75-78.[Web of Science][Medline]
Krebs JR, Davies NB, 1993. An introduction to behavioural ecology. Oxford: Blackwell Scientific.
Kunz TH, 1976. Observations of the winter ecology of the bat fly Trichobius corynorhini Cockerell (Diptera: Streblidae). J Med Entomol 12:631-636.[Web of Science][Medline]
Laurie WA, 1989. Effects of the 1982-83 El Niño-Southern Oscillation event on marine iguanas (Amblyrhynchus cristatus, Bell, 1825) populations in the Galápagos islands. In: Global ecological consequences of the 1982-83 El Niño-Southern Oscillation (Glynn P, ed). New York: Elsevier;121 -141.
Laurie WA, Brown D, 1990. Population biology of marine iguanas (Amblyrhynchus cristatus). 3. Factors affecting survival.J Anim Ecol 59:545-568.
Magurran AE, 1990. The adaptive significance of schooling as an anti-predator defence in fish. Ann Zool Fenn 27:51-66.
Matuschka FR, Richter D, Fischer P, Spielman A, 1990a. Nocturnal detachment of the tick Ixodes hexagonus from nocturnally active hosts. Med Vet Entomol 4:415-420.[Web of Science][Medline]
Matuschka FR, Richter D, Fischer P, Spielman A, 1990b. Time of repletion of subadult Ixodes ricinus ticks feeding on diverse hosts. Parasitol Res 76:540-544.[Web of Science][Medline]
Mooring MS, Hart BL, 1992. Animal grouping for protection from parasites: selfish herd and encounter-dilution effects.Behaviour 123:173-193.[Web of Science]
Nagy KA, Shoemaker VH, 1984. Field energetics and food consumption of the Galápagos marine iguana, Amblyrhynchus cristatus. Physiol Zool 57:281-290.
Noe R, Bshary R, 1997. The formation of red colobus-diana monkey associations under predation pressure from chimpanzees.Proc R Soc London Biol Sci 264:253-259.[Medline]
Oppliger A, Clobert J, 1997. Reduced tail regeneration in the common lizard, Lacerta vivipara, parasitized by blood parasites. Funct Ecol 11:652-655.
Packer C, Scheel D, Pusey AE, 1990. Why lions form groups: food is not enough. Am Nat 136:1-19.[Web of Science]
Poulin R, 1994. Meta-analysis of parasite-induced behavioural changes. Anim Behav 48:137-146.
Poulin R, FitzGerald GJ, 1989. Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.). Behav Ecol Sociobiol24 :251-255.
Prosser CL, Brown FA, 1965. Comparative animal physiology, 2nd ed. Philadelphia: WB Saunders.
Rassmann K, Tautz D, Trillmich F, Gliddon C, 1997. The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses. Mol Ecol 6:437-452.
Richner H, Opplinger A, Christe P, 1993. Effects of an ectoparasite on reproduction in great tits. J Anim Ecol 62:703-710.
Salvador A, Veiga JP, Martin J, Lopez P, Abelenda M, Puerta M,1996
. The cost of producing a sexual signal: testosterone
increases the susceptibility of male lizards to ectoparasitic infestation.Behav Ecol
7:145-150.
Schall JJ, 1990. The ecology of lizard malaria.Parasitol Today 6:264-269.
Schall JJ, Bennett AF, Putman RW, 1982. Lizards
infected with malaria: physiological and behavioral consequences.Science
217:1057-1059.
Schatz H, 1991. Catalogue of known species of acari from the Galápagos islands (Ecuador, Pacific Ocean). Int J Acarol 17:213-225.
Schmidt-Nielsen K, 1984. Scaling. Why is animal size so important? Cambridge: Cambridge University Press.
Sorci G, Clobert J, Michalakis Y, 1996. Cost of reproduction and cost of parasitism in the common lizard, Lacerta vivipara. Oikos 76:121-130.[Web of Science]
SPSS Inc. 1991. SPSS statistical algorithms, 2nd ed. Chicago: SPSS Inc.
Strassmann JE, 1992. Costs and benefits of colony aggregation in the social wasp Polistes annularis. Behav Ecol 2:204-209.[Web of Science]
Trillmich KGK, Trillmich F, 1986. Foraging strategies of the marine iguana, Amblyrhynchus cristatus. Behav Ecol Sociobiol 18:259-266.[Web of Science]
Underwood R, 1982. Seasonal changes in African ungulate groups. J Zool 196:191-205.[Web of Science]
Verdammen-Grandjean PH, 1966. Evolutionary problems of tick-host specificity and its relevance to studies on Galápagos organisms. In: The Galápagos (Bowman RI, ed). Berkeley: University of California Press;97 -123.
Wikelski M, Bäurle S,1996
. Pre-copulatory ejaculation solves time constraint during
copulations in marine iguanas. Proc R Soc Lond B
263:439-444.
Wikelski M, Carbone C, Trillmich F, 1996. Lekking in marine iguanas: female grouping and male reproductive strategies.Anim Behav 52:581-596.[Web of Science]
Wikelski M, Carrillo V, Trillmich F, 1997. Energy limits to body size in a grazing reptile, the Galápagos marine iguana.Ecology 78:2204-2217.[Web of Science]
Wikelski M, Gall B, Trillmich F, 1993. Ontogenetic changes in food-intake and digestion rate of the herbivorous marine iguana (Amblyrhynchus cristatus, Bell). Oecologia 94:373-379.[Web of Science]
Wikelski M, Hau M, 1995. Is there an endogenous tidal foraging rhythm in marine iguanas? J Biol Rhythms 10:345-360.
Wikelski M, Trillmich F, 1994. Foraging strategies of the Galápagos marine iguana (Amblyrhynchus cristatus): adapting behavioral rules to ontogenetic size change.Behaviour 128:255-279.[Web of Science]
Wikelski M, Trillmich F, 1997. Body size and sexual size dimorphism in marine iguanas fluctuate as a result of opposing natural and sexual selection: an island comparison. Evolution 51:922-936.[Web of Science]
Wittenberger JF, Hunt GL Jr, 1984. The adaptive significance of coloniality in birds. In: Avian biology, vol. 8 (Farner DS, King JR, eds). New York: Academic Press; 1-78.
Yuval, B, 1994. The vertebrate host as mating encounter site for its ectoparasites: Ecological and evolutionary considerations. Bull Soc Vector Ecol 19:115-120.
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