Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts

Sonia Kleindorfer; Rachael Y. Dudaniec

doi:10.1186/s40850-016-0003-9

Table 1 Overview of 31 studies to date examining the ecology, behavior and genetics of the Darwin’s finch Philornis downsi host-parasite system since the first discovery of P. downsi larvae in Darwin’s finch nests on Santa Cruz Island, Galápagos Archipelago, in 1997. Shown are data for 1) Number of finch host species or species name when singular, 2) Island, 3) Year study undertaken, 4) Sample size of nests (including number of control versus experimental [Exp.] nests), 5) P. downsi prevalence, 6) Mean number and range of P. downsi (in unmanipulated nests), 7) Percentage of in-nest mortality of nestlings in unmanipulated nests, 8) Effects on host, 9) Additional comments, 10) Type of study (Ecology, Genetics, Behavior), 11) Experimental study (E) versus Observational study (O), 12) Reference

From: Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts

1) Host species	2) Island	3) Year of study	4) Sample size	5) P. downsi prevalence	6) Mean number of P. downsi per nest (range)	7) In-nest mortality (%)	8) Effects on host	9) Comments	10) Type of Study	11) Exp. (E) versus Obs. (O) study	12) Reference
9 species	Santa Cruz	1998	63	97 %			N/A	First study to describe P. downsi in bird nests on Santa Cruz Island	Ecology	O	Fessl, Couri, Tebbich 2001 [29]
12 species	Santa Cruz	1998–2000	177	97 %	15.7 ± 7.4–49.8 ± 31.2 (0–182)	27 %	Number of larvae increased with nestling age; P. downsi not found in nests during incubation	Intensity compared for nestling age <8 days vs. >8d; species differed in intensity	Ecology	O	Fessl, Tebbich 2002 [28]
3 Darwin’s finch species	Santa Cruz	2000, 2004, 2005	63	100 %		−32.4–95.2 %	Damage to nestling nasal cavities; calculated 18–55 % overnight blood loss in nestlings due to parasitism	Identify two stage life cycle of P. downsi with 1st instar within nestling nares and 2nd and 3rd instar feeding externally	Ecology	O	Fessl, Sinclair, Kleindorfer 2006 [42]
2 Darwin’s finch species	Santa Cruz	2000, 2004	27	100 %	18.4 ± 2.4–23.2 ± 4.2	66 %	Parasitized nestlings had 61 % lower survival, 56 % lower body mass, 28 % lower hemoglobin concentration	11 nests prayed with 1 % permethrim (~1 P. downsi left per nest; range 0–5 larvae)	Ecology	E	Fessl, Kleindorfer, Tebbich 2006 [41]
Darwin’s finches	All islands						P. downsi given highest risk ranking for invasive species that negatively impact endemic fauna	23 % (around 463 species) of Galapagos invertebrate species are introduced of which 6 are confirmed to be highly invasive and harmful to endemic species	Ecology		Causton, Peck, Sinclair, Roque-Albelo, Hodgson, Landry 2006 [26]
Small ground finch	Santa Cruz, Floreana, Isabela	2004	24	92 %	23 ± 6 (0–90)		2 % lower hemoglobin concentration per additional larva	Effect of clutch size on P. downsi number per nestling	Ecology	O	Dudaniec, Kleindorfer, Fessl 2006 [44]
6 Darwin’s finch species	Santa Cruz	1998–2005	131	100 %	30.2 ± 4–66.8 ± 7.6	55 %	Positive association between P. downsi intensity and rainfall (eight year study); same intensity across habitats on Santa Cruz	Species differences in intensity	Ecology	O	Dudaniec, Fessl, Kleindorfer 2007 [33]
Darwin’s finches	13 islands	1998–2005	515		27.0 (1–182)		P. downsi was found on 11 of 13 islands sampled (absent from flat arid islands); more parasites in highland nests on elevated islands	Lowland nests on elevated islands had more P. downsi than lowland nests on flat islands	Ecology	O	Wiedenfeld, Jiménez, Fessl, Kleindorfer, Valarezo 2007 [39]
5 Darwin’s finch species	Santa Cruz, Floreana, Isabela	2004–2006	64	100 %			High gene flow between islands; some genetic differentiation of P. downsi on Floreana; evidence for genetic bottleneck	Sequenced CO1 mitochondrial gene fragments	Genetics, Ecology	O	Dudaniec, Gardner, Donnellan, Kleindorfer 2008 [40]
Medium ground finch	Santa Cruz	2004–2006	63	64–98 %	(0–200)	16–37 %	Number of P. downsi per nestling (but not per nest) predicted survival; no effect of P. downsi on nestling size	Nests earlier in the breeding season had more P. downsi per nest	Ecology	O	Huber 2008 [34]
Small ground finch	Santa Cruz	2008	623				36.3 % of adult birds had malformed beaks with enlarged naris (likely caused by P. downsi during the nestling phase)		Ecology	O	Galligan, Kleindorfer 2009 [48]
5 Darwin’s finch species	Santa Cruz	2000–2004	43	100 %	23.0 ± 3–57.0 ± 4		Larger finches built larger nests; within species, larger nests had more P. downsi		Behavior	O	Kleindorfer, Dudaniec 2009 [90]
Small ground finch	Floreana	2004–2006	39	94 %	8.0 ± 1.6–39.3 ± 4.6 (0–78)	3–33.4 %	Arid lowland nests had 80 % fewer P. downsi and 91 % lower in-nest mortality than highland nests		Ecology	O	O’Connor, Dudaniec, Kleindorfer 2010 [89]
Medium ground finch	Santa Cruz, Daphne Major	2008	67				More Philornis-specific antibodies in females than males, and more during the nesting period	No P. downsi found on Daphne Major	Ecology, Behavior	O	Huber, Owen, Koop, King, Grant, Grant, Clayton 2010 [46]
3 Darwin’s finch species	Santa Cruz, Floreana	2008	11	89 %	27.1 ± 8.5 (0–74)	79.2 %	Multiple P. downsi entries into the nest during incubation and feeding; nestlings stood on top of each other presumably to avoid larvae; adults preened nestling nares and nest base; nestling consumed larva	In-nest video; altered time budgets and behavior in heavily parasitized nests; adults removed dead nestling from nest	Behavior, Ecology	O	O’Connor, Robertson, Kleindorfer 2010 [49]
5 Darwin’s finch species	Santa Cruz, Floreana	2004–2006	57	100 %	30.8 ± 16.5 (5–65)		Genetic relatedness among P. downsi within nests was 57 % lower on Santa Cruz than on Floreana Island; between 1–6 different females laid their eggs per finch nest; each female mated with ~2 different males; each female laid ~5 eggs per finch nest with a maximum of 24 from one female		Genetics, Ecology, Behavior	O	Dudaniec, Gardner, Kleindorfer 2010 [117]
Medium tree finch	Floreana	2006, 2008	30	100 %	43.1 ± 10.7–65.6 ± 8.5 (8–96)	20–38 % total brood loss; 53 % of nests with partial or total brood loss	Parasite intensity did not predict fledging success; parasitized nestlings had grossly enlarged nares and tissue loss	Highest P. downsi intensity in critically endangered medium tree finch	Ecology	O	O’Connor, Sulloway, Robertson, Kleindorfer 2010 [38]
Mangrove finch	Isabela	2006–2009	15	100	40.8 ± 15.3 sd	14 %	Less rat predation after rat control (30 % predation after control versus 54 % predation before); P. downsi explained 14 % nestling mortality	Before and after rat control	Ecology	O + E	Fessl, Young, Young, Rodríguez-Matamoros, Dvorak, Tebbich 2010 [63]
Medium ground finch	Santa Cruz	2008	48	90 %	37.5 ± 4.9	96 %	Parasitized nestlings had ~30 % shorter primary feather length and 88 % lower fledging success	Nylon stocking placed over wire hoop as barrier to P. downsi; reduced parasite intensity to ~21 larvae per nest	Ecology, Behavior	E	Koop, Huber, Laverty, Clayton 2011 [63]
Darwin’s finches	All islands	2012-present					Summary of known P. downsi biology and impacts on endemic land birds	Launch of the P. downsi Action Plan	Ecology, Behavior, Genetics		Causton, Cunninghame, Tapia 2013 [72]
Medium ground finch	Santa Cruz	2010	30 (15 control, 15 exp.)		44.7 ± 6 (5–79)		No effect of P. downsi on attending female corticosterone level, body condition or hematocrit level	15 nests sprayed with 1 % permethrin (~0 per nest)		E	Knutie, Koop, French, Clayton 2013 [102]
Medium ground finch	Santa Cruz	2010	43 (22 control,21 exp)	100 %	38.5 ± 5.1	100 %	Compared with fumigated nests, females at parasitized nests had more P. downsi-specific antibodies, spent 42 % less time brooding and 74 % more time standing erect in the nest	14 females and 10 males from fumigated nests, 15 females and 10 males from parasitized nests	Behavior	E	Koop, Owen, Knutie, Aguilar, Clayton 2013 [47]
Medium ground finch	Santa Cruz	2009	13 (7 control, 6 exp.)	83 %	30.5 ± 7.5	86 %	No effect of rainfall on P. downsi intensity (two year study)	6 nests sprayed with 1 % permethrin (zero P. downsi)	Ecology	E	Koop, Le Bohec, Clayton 2013 [88]
Small ground finch	Floreana	2010	14 (7 control, 7 exp.)	100 %	22.7 ± 3.9 (12–60)	100 %	In-nest video; heavily parasitized nestlings had weak begging; parents only fed strongly begging nestlings	7 nests sprayed with 1 % permethrin (zero P. downsi)	Behavior	E	O’Connor, Robertson, Kleindorfer 2014 [100]
4 Darwin’s finch species	Floreana	2004–2013	238	100 %	27.5 ± 4.6 (2004) to 48.4 ± 6.5 (2013)	50–90 %	Across the decade, P. downsi intensity increased (~28 to ~48), in-nest mortality increased (~50 to ~90 %), nestlings died younger (~11 to ~5 days after hatching); pupa size got 10 % smaller (~10 mm to ~9 mm)	Compared with other finches, small ground finch nests had more P. downsi pupae, which indicates higher fly reproductive success	Ecology	O	Kleindorfer, Peters, Custance, Dudaniec, O’Connor 2014 [37]
3 Darwin’s tree finch species	Floreana	2005, 2010	201	100 %	25 ± 3–65 ± 18		Hybrid finch nests had 50–79 % fewer P. downsi than medium tree finch (2005, 2010)	Contemporary hybridization in Darwin’s tree Finches; evidence for hybrid fitness	Behavior, Genetics, Ecology	O	Kleindorfer, O’Connor, Dudaniec, Myers, Robertson, Sulloway 2014 [7]
2 Darwin’s finch species	Santa Cruz	2010, 2012	82	100 %	25, 38	37–56 %	Extreme weather events and number of P. downsi influenced nesting success	Species differences in P. downsi intensity	Ecology	O	Cimadom, Ulloa, Meidl, Zöttl, Zöttl, Fessl, Nemeth, Dvorak, Cunninghame, Tebbich 2014 [36]
4 Darwin’s finch species	Santa Cruz	2013	37 (17 control, 20 exp.) plus 26 nests checked for treated cotton		17 ± 3.9	46 %	Parasitized nests had 35 % lower fledging success	Permethrin-treated cotton from dispensers in 22 nests; 20 nests sprayed with 1 % permethrin (zero P. downsi)	Ecology	E	Knutie, McNew, Bartlow, Vargas, Clayton 2014 [70]
Small ground finch	Floreana	2010	14 (8 control, 6 exp.)	100 %	24.2 ± 2.7		Parasitized nestlings had larger relative (39 %) and absolute (3.3 mm) naris size compared with parasite-free nestlings (20.2 %, 1.6 mm)	6 nests sprayed with 1 % permethrin (zero P. downsi); museum specimens had normal naris size suggesting post 1960s arrival of P. downsi	Ecology, Morphology	E	Kleindorfer, Sulloway 2016 [30]
3 Darwin’s finch species	Floreana	2004–2014	582	100 %	17.7 ± 3.3–87.8 ± 19.5		Higher fly traps caught more female P. downsi; higher finch nests had more P. downsi	28 McPhail traps placed at 1 m–7 m to test for fly sex ratio at different trapping heights	Behavior, Ecology	E	Kleindorfer, Peters, Hohl, Sulloway 2016 [71]
Medium ground finch, mockingbird	Santa Cruz	2012, 2013	127				P. downsi density (grams per nestling g) predicted finch but not mockingbird mortality; no P. downsi antibodies in nestlings; parasitized mockingbird but not finch nestlings begged more	32 finch nests and 34 mockingbird nests prayed with 1 % permethrin	Behavior, Ecology	E	Knutie, Owen, McNew, Bartlow, Arriero, Herman, DiBlasi, Thompson, Koop, Clayton 2016 [105]

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