FunctionalEcology200519, 625–631© 2

Functional
Ecology
2005
19
, 625–631
© 2005 British
Ecological Society
625
Blackwell Publishing, Ltd.
Is a starving host tastier? Reproduction in fleas
parasitizing food-limited rodents
B. R. KRASNOV,*† I. S. KHOKHLOVA,‡ M. S. ARAKELYAN*§ and
A. A. DEGEN‡
*
Ramon Science Center and Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research,
Ben-Gurion University of the Negev, Mizpe Ramon, Israel,
‡
The Wyler Department of Dryland Agriculture, Jacob
Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Israel, and
§
Department of Zoology, Yerevan State University, Yerevan, Armenia
Summary
1.
We hypothesized that food availability, and therefore body condition, of a rodent
host,
Meriones crassus
, affects egg production and survival, and development time of
preimago and adults of the first generation of the flea
Xenopsylla ramesis
.
2.
Egg production was significantly higher in fleas parasitizing underfed than control
animals.
3.
Food availability for hosts affected survival of eggs and larvae produced by fleas on
these rodents, but did not affect survival of pupae. More than twice the number of eggs
from fleas on food-limited hosts survived than those from fleas on control rodents.
Highest larval survival was recorded in fleas on rodents with 30% of maintenance
energy intake.
4.
Survival of new generation imagos was lowest in fleas from parents on hosts with
the highest food limitation. By contrast, survival of parent fleas was highest on hosts
offered 30% of maintenance energy intake.
5.
Time of egg and larval development was longest on hosts consuming 30% of energy
requirements for maintenance. By contrast, there was no difference in time to emergence
in pupae from flea females on rodents from different treatments. Survival time
under starvation of imago of the first generation was shortest in offspring of fleas that
parasitized
M. crassus
offered the minimal amount of food. The opposite was true for
parent fleas.
6.
The results suggest nutritional and/or energetic cost of host resistance, measured
as host-mediated parasite fitness loss, as well as possible adaptive stress-induced
immunosuppression.
Key-words
: Egg production, flea, food limitation, rodent host, survival
Functional Ecology
(2005)
19
, 625–631
doi: 10.1111/j.1365-2435.2005.01015.x
Introduction
Distribution of parasite individuals across a host
population is characterized by their aggregation. Most
individuals of the parasite occur on a few host individuals,
while most host individuals have only a few, if any,
parasites (Anderson & May 1978). The general cause
of the heterogeneous distribution of parasites is due to
host heterogeneity of the rate of gain or loss of parasites
(Poulin 1998). In other words, if some hosts have more
parasites than would be predicted by chance, it suggests
that they offer the parasites a better quality habitat. In
particular, intraspecific host variation in suitability for
a parasite can be caused by the variation in the pattern
of resource acquisition by a parasite such as intrahost
variation in defences.
Hosts defend themselves against parasites using
specific behavioural, physiological and/or immunological
mechanisms that can result in loss of fitness in the
parasites. This host-mediated loss of fitness in a parasite
is considered to be host resistance (Poulin 1998). The
defence against parasites can be costly for a host. For
example, activation of an immune response and even
maintenance of a competent immune system is an energetically
demanding process that requires trade-off decisions
among competing energy demands for growth,
†Author to whom correspondence should be addressed.
E-mail: [e-mail]
626
B. R. Krasnov
et al.
© 2005 British
Ecological Society,
Functional Ecology
,
19
, 625–631
reproduction, thermoregulation, work and immunity
(Sheldon & Verhulst 1996). Empirical evidence suggests
that such costs can be high (e.g. Moret & Schmid-
Hempel 2000).
The trade-off between the advantage of resistance
and its cost should be most critical for hosts that face
energy limitations. Therefore, energy-deprived hosts
might be less resistant and, thus, represent better patches
for parasites. Intraspecific host variation in energy reserves
can arise due to a variety of reasons (Kam & Degen 1993;
Cumming & Bernard 1997). As a result, in many nontropical
vertebrate animals, disease prevalence is increased
during periods of food shortage compared with periods
when food is readily available (Lochmiller, Vestey &
McMurray 1994). However, resources that parasites
extract from their hosts (e.g. blood) can be of a lower
quality in energy-deprived hosts (De Pedro
et al
. 2003).
Thus, hosts in good condition can be a better food source
than hosts in poor condition (Dawson & Bortolotti 1997).
Consequently, parasites face a trade-off between the
choice to attack less defended but lower-quality,
vs
more
defended but higher-quality, hosts. From the evolutionary
perspective, the strategy of parasitizing either
energy deprived or energy-rich hosts would depend on
relative fitness rewards from exploiting these hosts.
This reasoning leads to two alternative predictions
regarding the effect of host energy deprivation on
reproductive patterns of a parasite. Reproductive output
of a parasite will be higher when exploiting energy
deprived hosts if the fitness increment due to reduced
host defences is higher than the fitness decline due to
lower quality of resources extracted from a host.
Alternatively, this reproductive output will be lower
when exploiting energy deprived hosts if the fitness
increment due to reduced host defences is lower than
the fitness decline due to lower quality of extracted
resources.
The effect of body condition of hosts on their
resistance to parasites has been studied in a variety of
animals by manipulating the body condition of hosts
(Oppliger, Christe & Richner 1996; Brown, Loosli &
Schmid-Hempel 2000; Jokela
et al
. 2005). However, all
of these studies have investigated this phenomenon from
the host perspective, whereas the effect of host condition
on parasite parameters (apart for abundance) has largely
been neglected.
Here, we studied the effect of host energy intake on
parasite fitness. We hypothesized that food limitation
of a rodent host,
Meriones crassus
, affects reproductive
potential (in terms of egg production) and quality of
offspring (in terms of survival and development time
of preimaginal stages and adults of the first generation)
of its characteristic flea parasite
Xenopsylla ramesis
.
Fleas (Siphonaptera) are parasites of higher vertebrates,
being most abundant and diverse on small mammals.
In most cases, preimaginal development is entirely
off-host. Larvae of almost all flea species are not
parasitic and feed on organic debris in the burrow and/
or nest of the host.
Materials and methods
    
Fleas and rodents (27 adult males) were obtained from
our laboratory colonies started from field-collected
individuals. Details on the flea and rodent-rearing
procedures can be found elsewhere (Krasnov
et al
.
2001a,b, 2004). In this study we used only newly emerged
fleas, 2 days of age, which did not feed from emergence
until experimental treatments. The study was conducted
under permits from the Israel Nature and National
Parks Protection Authority and Ben-Gurion University
Committee for the Ethical Care and Use of Animals in
Experiments.
  
Prior to experimental trials with fleas, the rodents were
placed in individual plastic cages (20
×
40
×
15 cm
3
with
3 mm clean sand as a substrate) and divided randomly
into three groups (nine individuals per group). One group
(control group, C) was offered millet seeds equivalent to
approximately 100% of maintenance energy requirements,
whereas the two other groups were offered
60% (group T1) and 30% (group T2), respectively, of
maintenance requirements. In addition, rodents were
offered 3 g fresh alfalfa leaves, which provided their water
needs but with minimal additional energy (I. Khokhlova,
unpublished data). Energy requirements for maintenance
of
M. crassus
were taken as 8·3 kJ day
−
1
(Khokhlova, Degen & Kam 1995) and calculated for
each animal based on its body mass (
m
b
). Animals were
weighed daily at 09.00 h to 0·01 g (Ohaus CT200-S
electronic balance, Ohaus Corporation, Pine Brook, NJ,
USA). Food offered was weighed to 0·0001 g (Mettler-
Toledo AB, Dietikon, Switzerland). Animals from the
control group and animals from the T1 treatment
maintained their body mass throughout the experimental
period; their body mass after the first week was
98·9
±
2·1% and 97·3
±
1·7%, respectively, of initial
body mass. However, body mass of rodents from the
T2 group decreased after the first week to 81·1
±
1·8%
of initial body mass.
  
We selected 945 newly emerged female and 270 newly
emerged male
X. ramesis
and assigned them randomly
to the three experimental treatments that differed in
food availability to a rodent host. We placed 35 female and
10 male fleas on each rodent a week after the beginning
of experiments. Four days after the fleas were in the
rodent cage, we collected the fleas by brushing the hair
of the rodent with a toothbrush and sieving the cage
substrate until no fleas could be recovered during
10 min of either brushing or sieving. No behavioural
difference during manipulations was recorded among
rodents of the three experimental groups. In total, we
mb
−0⋅54
627
Reproduction in
fleas exploiting a
food-limited host
© 2005 British
Ecological Society,
Functional Ecology
,
19
, 625–631
recovered 804 female and 156 male fleas. Each female
flea was examined under a light microscope, and the
degree of egg development (early, middle or late stage)
was determined visually (see Krasnov
et al
. 2002 for
details). Fleas with egg

Results (Indonesian) 1:

FungsionalEkologi200519625-631© 2005 BritishEcological Society625Blackwell penerbitan, LtdApakah sebuah host yang kelaparan lebih lezat? Reproduksi di kutuparasitizing makanan terbatas tikusB. R. KRASNOV, * † I. S. KHOKHLOVA, ‡ M. S. ARAKELYAN * § danA. A. DEGEN‡*Ramon Science Center dan Mitrani Departemen gurun ekologi, lembaga-lembaga penelitian Desert, Jacob BlausteinUniversitas Ben-Gurion Negev, Mizpe Ramon, Israel,‡Departemen Wyler dan pertanian, YakubBlaustein lembaga-lembaga penelitian Desert, Ben-Gurion University of the Negev, Sede Boqer kampus, Israel, dan§Departemen Zoologi, Universitas negara Yerevan, Yerevan, ArmeniaRingkasan1.Kami hipotesis bahwa ketersediaan pangan, dan karena itu tubuh kondisi, rodenttuan rumah,Meriones crassus, mempengaruhi telur waktu produksi dan kelangsungan hidup, dan pengembanganpreimago dan orang dewasa dari generasi pertama kutuXenopsylla ramesis.2.Produksi telur adalah signifikan lebih tinggi di kutu parasitizing kurang makan dari kontrolhewan.3.Ketersediaan pangan untuk host mempengaruhi kelangsungan hidup telur dan larva yang diproduksi oleh kutu padatikus ini, tetapi tidak mempengaruhi kelangsungan hidup kepompong. Lebih dari dua kali jumlah telurdari kutu pada makanan-terbatas host selamat daripada dari kutu pada pengendalian tikus.Kelangsungan hidup larva tertinggi tercatat di kutu pada tikus dengan 30% dari pemeliharaanasupan energi.4.Kelangsungan hidup generasi baru imagos yang terendah di kutu dari orangtua pada host denganbatasan makanan yang tertinggi. Sebaliknya, kelangsungan hidup kutu orangtua adalah tertinggi pada hostditawarkan 30% dari asupan energi pemeliharaan.5.Waktu telur dan perkembangan larva adalah terpanjang di host mengkonsumsi 30% dari energipersyaratan untuk pemeliharaan. Sebaliknya, ada tidak ada perbedaan dalam waktu untuk timbulnyadalam kepompong dari loak betina pada tikus dari perawatan yang berbeda. Waktu kelangsungan hidupdi bawah kelaparan imago generasi pertama adalah terpendek dalam keturunan kutu yangparasitizedM. crassusminimal jumlah makanan yang ditawarkan. Sebaliknya adalah benar untukorangtua kutu.6.Hasilnya menunjukkan biaya gizi dan/atau energik resistensi host, diukursebagai tuan rumah-dimediasi parasit kebugaran kerugian, serta mungkin adaptif diinduksi stresimunosupresi.Kata kunci: Telur produksi, kutu, batasan makanan, hewan pengerat host, kelangsungan hidupEkologi fungsional(2005)19625-631Doi: 10.1111/j.1365-2435.2005.01015.xPendahuluanDistribusi parasit individu di seluruh hostpopulasi dicirikan oleh agregasi mereka. Sebagianindividu parasit terjadi pada beberapa host individuSementara kebanyakan host individu memiliki hanya sedikit, jika ada,parasit (Anderson & Mei 1978). Penyebab umumdistribusi heterogen parasit adalah karenahost heterogenitas tingkat keuntungan atau kerugian parasit(Poulin 1998). Dengan kata lain, jika beberapa host memiliki lebihparasit daripada akan dapat diprediksi secara kebetulan, itu menyarankanbahwa mereka menawarkan parasit habitat kualitas lebih baik. Dalamkhusus, intraspecific host variasi dalam kesesuaian untukparasit dapat disebabkan oleh variasi dalam polasumber daya akuisisi oleh parasit seperti intrahostvariasi dalam pertahanan.Host membela diri terhadap parasit menggunakanspesifik perilaku, fisiologis dan/atau imunologimekanisme yang dapat mengakibatkan kerugian kebugaran diparasit. Kerugian ini host-dimediasi kebugaran di parasitini dianggap untuk menjadi tuan rumah perlawanan (Poulin 1998). Thepertahanan terhadap parasit dapat menjadi mahal bagi tuan rumah. Untukcontoh, aktivasi respon imun dan bahkanpemeliharaan sistem kekebalan tubuh yang kompeten yang penuh semangatmenuntut proses yang memerlukan trade-off keputusandi antara tuntutan energi yang saling bersaing untuk pertumbuhan,†Author kepada siapa korespondensi harus ditangani.E-mail: [e-mail]626B. R. Krasnovet al.© 2005 BritishEcological Society,Ekologi fungsional,19625-631reproduksi, Termoregulasi hewan, pekerjaan dan imunitas(Sheldon & Verhulst 1996). Bukti empiris menunjukkanbahwa biaya tersebut bisa tinggi (misalnya Moret & Schmid -Hempel 2000).Trade-off antara keuntungan dari perlawanandan biaya harus paling kritis untuk host-host yang dihadapiketerbatasan energi. Oleh karena itu, kekurangan energi hostmungkin kurang tahan dan, dengan demikian, mewakili patch lebih baikuntuk parasit. Intraspecific host variasi dalam energi cadangandapat timbul karena berbagai alasan (Kam & Degen 1993;Cumming & Bernard 1997). Sebagai akibatnya, di banyak nontropicalvertebrate animals, disease prevalence is increasedduring periods of food shortage compared with periodswhen food is readily available (Lochmiller, Vestey &McMurray 1994). However, resources that parasitesextract from their hosts (e.g. blood) can be of a lowerquality in energy-deprived hosts (De Pedroet al. 2003).Thus, hosts in good condition can be a better food sourcethan hosts in poor condition (Dawson & Bortolotti 1997).Consequently, parasites face a trade-off between thechoice to attack less defended but lower-quality,vsmoredefended but higher-quality, hosts. From the evolutionaryperspective, the strategy of parasitizing eitherenergy deprived or energy-rich hosts would depend onrelative fitness rewards from exploiting these hosts.This reasoning leads to two alternative predictionsregarding the effect of host energy deprivation onreproductive patterns of a parasite. Reproductive outputof a parasite will be higher when exploiting energydeprived hosts if the fitness increment due to reducedhost defences is higher than the fitness decline due tolower quality of resources extracted from a host.Alternatively, this reproductive output will be lowerwhen exploiting energy deprived hosts if the fitnessincrement due to reduced host defences is lower thanthe fitness decline due to lower quality of extractedresources.The effect of body condition of hosts on theirresistance to parasites has been studied in a variety ofhewan dengan memanipulasi kondisi tubuh host(Oppliger, Christe & Richner 1996; Coklat, Loosli &Schmid-Hempel 2000; Jokelaet al. 2005). Namun, Semuastudi ini menyelidiki fenomena ini dariperspektif tuan rumah, sedangkan efek host kondisipada parameter parasit (terpisah untuk kelimpahan) telah sebagian besartelah diabaikan.Di sini, kita mempelajari efek dari asupan energi host padaKebugaran parasit. Kami dihipotesiskan keterbatasan makanan yangdari sejumlah hewan pengerat,Meriones crassus, mempengaruhi reproduksipotensi (dalam hal produksi telur) dan kualitasketurunan (dalam hal waktu kelangsungan hidup dan pengembangantahapan preimaginal dan orang dewasa dari generasi pertama)dengan karakteristik kutu parasitXenopsylla ramesis.Kutu (Siphonaptera) adalah parasit vertebrata yang lebih tinggi,yang paling berlimpah dan beragam pada mamalia kecil.Dalam kebanyakan kasus, pengembangan preimaginal adalah sepenuhnyaoff-host. Larva hampir semua spesies loak tidakparasit dan feed di puing-puing organik dalam Liang dan /atau sarang host.Bahan dan metode    Kutu dan hewan pengerat (27 jantan dewasa) Diperoleh darikoloni laboratorium kita mulai dari bidang yang dikumpulkanindividu. Rincian tentang flea dan membesarkan rodentprosedur dapat ditemukan di tempat lain (Krasnovet al.2001a, b, 2004). Dalam studi ini, kita digunakan hanya baru munculkutu, 2 hari usia, yang tidak memberi makanan dari munculnyasampai perawatan eksperimental. Penelitian inidi bawah izin dari alam Israel dan nasionalTaman perlindungan otoritas dan Ben-Gurion UniversityKomite untuk perawatan etis dan penggunaan hewan diPercobaan.  Sebelum percobaan percobaan dengan kutu, tikus yangditempatkan dalam kandang plastik individu (20×40×15 cm3dengan3 mm membersihkan pasir sebagai substrat) dan dibagi secara acakmenjadi tiga kelompok (sembilan individu per grup). Satu kelompok(kelompok kontrol, C) ditawarkan millet benih setara dengansekitar 100% dari kebutuhan energi pemeliharaan,Sedangkan dua kelompok lain yang ditawarkan60% (kelompok T1) dan 30% (kelompok T2), masing-masing, daripersyaratan pemeliharaan. Selain itu, tikus yangdaun alfalfa segar ditawarkan 3 g, yang menyediakan air merekakebutuhan, tetapi dengan sedikit tambahan energi (I. Khokhlova,Diterbitkan data). Kebutuhan energi untuk pemeliharaandariM. crassusdiambil sebagai 8·3 kJ hari−1(Khokhlova, Degen & Kam 1995) dan dihitung untukmasing-masing hewan berdasarkan (massa tubuh yangmb). Binatang ituditimbang setiap hari jam 09.00 h untuk 0·01 g (Ohaus CT200-Selektronik keseimbangan, Ohaus Corporation, Pine Brook, NJ,USA). Makanan yang ditawarkan ditimbang untuk 0·0001 g (Mettler-Toledo AB, Dietikon, Swiss). Hewan darikelompok kontrol dan hewan dari perlakuan T1mempertahankan massa tubuh mereka seluruh percobaanperiode; massa tubuh mereka setelah minggu pertama98·9±2·1% dan 97·3±1·7%, masing-masing, dari awalmassa tubuh. Namun, massa dari tikus dari tubuhT2 Grup menurun setelah minggu pertama hingga 81·1±1·8%dari awal massa tubuh.  Kami memilih 945 baru muncul perempuan dan 270 barumuncul laki-lakiX. ramesisdan mereka ditugaskan secara acakuntuk perawatan eksperimental tiga yang berbeda dalamketersediaan pangan sejumlah hewan pengerat. Kami menempatkan 35 perempuan dan10 laki-laki kutu pada setiap rodent seminggu setelah awalpercobaan. Empat hari setelah kutu berada dikandang hewan pengerat, kami mengumpulkan kutu dengan menyikat rambutdari hewan dengan sikat gigi dan sieving kandangsubstrat sampai tidak ada kutu bisa pulih selama10 min menyikat atau analisa saringan. Tidak perilakuperbedaan selama manipulasi direkam antaratikus dari tiga kelompok eksperimental. Secara total, kamiMB−0⋅54627Reproduksi dalamkutu mengeksploitasihost makanan terbatas© 2005 BritishEcological Society,Ekologi fungsional,19625-631pulih 804 perempuan dan 156 kutu laki-laki. Laki-laki masing-masingFlea diteliti di bawah mikroskop cahaya, dangelar telur pembangunan (tahap awal, tengah atau akhir)ditentukan secara visual (Lihat Krasnovet al. 2002 untukrincian). Kutu dengan telur